NeuroImage 49 (2010) 865–874

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NeuroImage
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y n i m g

A common functional brain network for autobiographical, episodic, and semantic

memory retrieval
Hana Burianova a,b,⁎, Anthony R. McIntosh a,b, Cheryl L. Grady a,b,c
a
Department of Psychology, University of Toronto, Toronto, Ontario, Canada
b
Rotman Research Institute at Baycrest, Toronto, Ontario, Canada
c
Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada

a r t i c l e i n f o a b s t r a c t

Article history: The objective of this study was to delineate a common functional network that underlies autobiographical,
Received 22 April 2009 episodic, and semantic memory retrieval. We conducted an event-related fMRI study in which we utilized
Revised 9 August 2009 the same pictorial stimuli, but manipulated retrieval demands to extract autobiographical, episodic, or
Accepted 31 August 2009
semantic memories. To assess this common network, we first examined the functional connectivity of
Available online 8 September 2009
regions identified by a previous analysis of task-related activity that were active across all three tasks. Three
of these regions (left hippocampus, left lingual gyrus, and right caudate nucleus) appeared to share a
common pattern of connectivity. This was confirmed in a subsequent functional connectivity analysis using
these three regions as seeds. The results of this analysis showed that there was a pattern of functional
connectivity that characterized all three seeds and that was common across the three retrieval conditions.
Activity in inferior frontal and middle temporal cortex bilaterally, left temporoparietal junction, and anterior
and posterior cingulate gyri was positively correlated with the seeds, whereas activity in posterior occipito-
temporo-parietal regions was negatively correlated. These findings support the idea that a common neural
network underlies the retrieval of declarative memories regardless of memory content. This proposed
network consists of increased activity in regions that represent internal processes of memory retrieval and
decreased activity in regions that mediate attention to external stimuli.
© 2009 Elsevier Inc. All rights reserved.

Introduction multiple memory systems view of the organization of declarative

Despite extensive research in the past several decades, a consensus
has yet to be reached as to the neural organization of declarative
memory retrieval. Conceptually, declarative memory retrieval has
been traditionally dissociated into three types: (1) semantic retrieval,
characterized by the conscious recollection of factual information and
general knowledge (Tulving, 1972); (2) episodic retrieval, character-
ized by the conscious recollection of experienced events, which
originally included personally relevant events (Tulving, 1972), but
today typically pertains to memory for stimuli encoded in the
laboratory (i.e., ”laboratory memory”; see Cabeza and St. Jacques,
2007); and (3) autobiographical retrieval, characterized by the
conscious recollection of personally relevant events (Conway and
Pleydell-Pearce, 2000). Much of the data from neuropsychological and
neuroimaging experiments (e.g., Cipolotti and Maguire, 2003; Gadian
et al., 2000; Hirano and Noguchi, 1998; Manns et al., 2003; Nyberg,
McIntosh and Tulving, 1998; Vargha-Khadem et al., 1997) support the
⁎ Corresponding author. Psychology Department, University of Toronto, 100 St.
George Street, Toronto, Ontario, Canada M5S 3G3.
E-mail address: hburian@rotman-baycrest.on.ca (H. Burianova).
memory (Tulving, 1987). This view posits that there are separate
memory systems, which specialize in the processing of distinct types
of information and recruit functionally independent neural networks,
each mediating a specific memory function (Cabeza and Nyberg,
2000; Gabrieli, 1998; Nyberg, McIntosh and Tulving, 1998; Nyberg et
al., 2002; Tulving and Schacter, 1990; Tulving, 1987). Empirical
evidence supporting this view comes primarily from studies showing
functional dissociations between episodic, autobiographical, and
semantic memory. Neuropsychological studies show that patients
with medial temporal lobe lesions are usually impaired on tasks
involving autobiographical memory, but not on tasks involving
semantic memory (Gadian et al., 2000; Hirano and Noguchi, 1998;
Vargha-Khadem et al., 1997), suggesting that the medial temporal
lobes (the hippocampus, in particular) engage autobiographical
memory exclusively (Tulving et al., 1991; Tulving and Markowitsch,
1998; Vargha-Khadem et al., 1997). Conversely, patients with
semantic dementia whose neural damage often involves frontotem-
poral lobar degeneration (Hodges and Miller, 2001; Neary et al., 1998)
are characterized by severe semantic memory loss, whereas their
autobiographical memory is relatively spared (Graham et al., 2003;
McKinnon et al., 2006; Snowden, Griffiths and Neary, 1994;
Westmacott and Moscovitch, 2003). Further neural dissociations

1053-8119/$ – see front matter © 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.neuroimage.2009.08.066
866 H. Burianova et al. / NeuroImage 49 (2010) 865–874
have been found in neuroimaging studies that show regional activity
in the left inferior prefrontal cortex and left posterior temporal areas
related to semantic retrieval (Graham et al., 2003; Vandenberghe et
al., 1996; Wiggs, Weisberg and Martin, 1999), left-lateralized activity
in the medial temporal and ventromedial frontal regions, tempor-
opolar areas, retrosplenial cingulate cortex, and cerebellum related to
autobiographical retrieval (Conway et al., 2002; Gilboa, 2004; Graham
et al., 2003; Maguire, 2001), and activity in the right dorsolateral
prefrontal areas subserving “laboratory” episodic retrieval (Duzel et
al., 2004; Gilboa, 2004). It is critical to point out, however, that the
focus of most of these neuropsychological and neuroimaging studies
was largely on differences and functional dissociations of autobio-
graphical, episodic, and semantic memory retrieval. In other words,
the experimental paradigms (e.g., using different tasks to test episodic
and semantic memory) and statistical methods (e.g., subtracting
activity during one memory condition from another, instead of using a
neutral baseline) were designed to dissociate neural correlates among
the presumably different types of declarative memory.
An alternative perspective to the multiple systems view is the
unitary system view of the organization of declarative memory, which
proposes the idea of a single declarative memory system (Baddley,
1984; Friston, 2002; Kihlstrom, 1984; McIntosh, 1999; Rajah and
McIntosh, 2005; Roediger, 1984). Proponents of this view conjecture
that a unitary memory system gives rise to all declarative memory
retrieval, although memories can vary along a contextual continuum
of several dimensions, such as time, space, emotion, or strength of
recollection (e.g., Baddley, 1984). This view rests on several
theoretical assumptions. Firstly, encoding of to-be-remembered
material is almost always contextual (i.e., embedded in already
attained knowledge; Baddley, 1984); at retrieval, memories may or
may not become decontextualized along one or more of these
dimensions (Baddley, 1984; Rajah and McIntosh, 2005; Westmacott
and Moscovitch, 2003). Autobiographical and semantic types of
memory may thus be conceptualized as the opposite ends of the
contextual continuum (Baddley, 1984; Kihlstrom, 1984; Roediger,
1984). Secondly, even if autobiographical memory is at the most
detailed end of the contextual continuum, it is not free of factual,
semantic information (Gilboa, 2004; Levine et al., 2002); hence, there
is considerable overlap among these ‘types’ of memory, and the
boundaries between them are often unclear. Finally, in a similar vein,
semantic memory is rarely entirely context-free, but rather contains
some contextual and episodic components, although these may be
degraded and lack rich detail (Gilboa, 2004; Westmacott and
Moscovitch, 2003; Westmacott et al., 2004).
Evidence supporting the unitary memory system view consists of
both neuroimaging and neuropsychological data that show functional
overlap and interdependence of different memory functions (Duncan
and Owen, 2000; Kopelman and Kapur, 2001; Manns et al., 2003;
Rajah and McIntosh, 2005; Squire and Zola, 1998). These include
studies comparing working, episodic, and semantic memory (Nyberg
et al., 2002, 2003), working and episodic memory (Braver et al., 2001;
Cabeza et al., 2002; Duzel et al., 1999), and semantic and episodic
memory (Rajah and McIntosh, 2005; Ryan et al., 2008), all of which
reported commonalities in neural activations across the memory
tasks. Rajah and McIntosh (2005) provided evidence for the unitary
view by modeling separate functional networks for episodic and
semantic retrieval tasks and assessing interregional correlations
across the two tasks. The results showed no significant differences
in the interregional correlations, despite differences in regional
activations in the two memory tasks, suggesting the involvement of
a single memory system or network. Other data (e.g., Moscovitch,
1992; Seger et al., 2000; Shimamura, 1995) contradict the prefrontal
hemispheric differentiation of episodic and semantic retrieval (i.e.,
activity in the right prefrontal cortex is associated solely with episodic
retrieval [Buckner et al., 1998; Cabeza and Nyberg, 2000] and activity
in the left prefrontal cortex is solely associated with semantic retrieval
[e.g., Goldberg et al., 2007]). In healthy individuals, activity in the right
prefrontal cortex was shown to underlie retrieval of novel and
creative semantic relations (Dobbins and Wagner, 2005; Seger et al.,
2000), whereas activity in the left prefrontal cortex was found to
subserve some aspects of episodic remembering (Nolde et al., 1998).
This support for the unitary view of declarative retrieval even
extends to the hippocampus, traditionally thought to subserve
episodic and autobiographical memory only (Tulving et al., 1991;
Tulving and Markowitsch, 1998; Vargha-Khadem et al., 1997). For
example, there is evidence that hippocampal amnesics, when
compared to healthy controls, exhibit impairments in semantic
retrieval in addition to profound deficits in episodic and autobio-
graphical retrieval (Kopelman and Kapur, 2001; Manns et al., 2003;
Squire and Zola, 1998). Similarly, recent imaging studies of healthy
individuals have reported hippocampal activation in both episodic
and semantic retrieval (e.g., Burianova and Grady, 2007; Ryan et al.,
2008). These data suggest that the hippocampus and the medial
temporal cortices are involved in all declarative retrieval.
In a previous study, we identified regional activations common to
autobiographical, “laboratory” episodic, and semantic retrieval (Bur-
ianova and Grady, 2007). While these results reflect the important
neural substrates that are involved in declarative retrieval, they do not
provide direct evidence about the functional connectivity of these
neural regions. It seems reasonable to assume that memory retrieval,
a highly complex cognitive process, would not be localized to discrete
brain region(s), but rather would be mediated by the interaction
among a number of functionally related neural areas. This idea is not
new, as many researchers have argued that it is the activity of
distributed neural networks and the interactions among anatomically
connected brain regions that directly yield cognitive functions, such as
memory (e.g., Finger, 1994; Friston, 1997; McIntosh, 1998, 2000;
Mesulam, 1990). In other words, cognitive functions are the emergent
properties of the neural interactions (i.e., influences that neural
constituents have on one another) among numerous brain areas that
comprise a neural network (McIntosh, 1999). An essential aspect of
the network approach to the neural organization of cognitive function
is the examination of the neural context associated with a specific
behaviour (McIntosh, 1998, 1999). Neural context is conceptualized
as the activity in a selected brain region that arises as a consequence of
modulatory influences from other brain regions (McIntosh, 1998,
1999). Thus, what is important in determining the neural underpin-
ning of a cognitive function is the relation of activity in a brain area
with activity of those brain areas with which it is connected. In
parallel with this argument is the notion that by measuring only how
mean neural activity changes with task in a specific brain area or
areas, one might fail to observe relevant interregional functional
interactions that occur despite no significant change in the mean
activity (e.g., Grady et al., 1998; McIntosh et al., 1994).
One approach to quantifying neural interactions is to assess the
degree of functional connectivity among brain regions, i.e., the degree
to which activity in a specific region correlates or covaries with
activity in other areas across the whole brain, thus functioning
together as a network (Friston et al., 1993; Friston, 1994; Horwitz et
al., 1984). A network is thus defined as a pattern of spatially remote
brain regions whose activity levels are correlated, or functionally
connected across participants, in order to support a particular
behaviour, regardless of whether the average level of activity in any
single region of the network is different between the experimental
conditions (Friston, 1994; Habib et al., 2003). To statistically study
complex neural interactions between different brain structures, the
analytical methods must provide a means to quantifying the relation
between brain regions, rather than focusing on mean activity
differences. Multivariate approaches, such as the partial least squares
(PLS) approach to image analysis, enable investigation of functional
connectivity of neural regions by calculating the covariance between
the activity within selected seed voxels and all other brain voxels
 H. Burianova et al. / NeuroImage 49 (2010) 865–874
across the experimental conditions (McIntosh et al., 1996; McIntosh
and Gonzalez-Lima, 1994). For instance, Addis et al. (2004a) identified
a number of autobiographical regions that differentiated general and
specific autobiographical memories from a control baseline using
univariate contrasts, but only a subsequent multivariate PLS analysis
(Addis et al., 2004b) revealed a shared functional network with a
critical connection to the hippocampus. Furthermore, Addis et al.
(2007) expanded on these findings by mapping an effective
autobiographical network in healthy individuals and epileptic
patients. In addition to Addis' work, other researchers have assessed
the autobiographical network (Levine et al., 2004; Maguire et al.
2001), pinpointing the interplay of frontal (medial, middle, inferior,
and superior frontal gyri) and temporal areas (temporal pole,
hippocampus, and parahippocampal gyrus), temporoparietal junc-
tion, retrosplenial cortex, and posterior cingulate gyrus. Episodic
retrieval of stimuli learned in the laboratory has been linked to a
functional network that overlaps to some degree with the autobio-
graphical network, but that also recruits unique brain regions, for
instance, the insula, occipito-temporal cortex, posterior parietal areas,
and precuneus (e.g., Nyberg et al., 2002; for a review see Gilboa et al.,
2004). Semantic memory processes have been generally reflected in
the inter-correlation of activity in a number of temporal regions
(inferior, middle, and superior temporal gyrus; Martin and Chao,
2001; Vandenberghe et al., 1996), as well as in an overlap with the
autobiographical network, particularly in the lateral temporal gyrus,
temporoparietal junction, anterior cingulate gyrus, and ventrolateral
prefrontal cortex (Lee et al., 2002; Mummery et al., 1996). However,
despite these explorations of the functional and effective connectivity
of the neural correlates that underlie declarative memory, no study to
date has attempted to identify a single network common to
autobiographical, episodic, and semantic retrieval in one experiment
and/or analysis.
The purpose of this study was to delineate a functional network of
spatially distributed neural regions whose activity covaries across the
three memory conditions, i.e., to map a common functional
declarative retrieval network. To do so, the data were analyzed
with seed voxel PLS analysis (Della-Maggiore et al., 2000; McIntosh,
1999; McIntosh et al., 1997; Schreurs et al., 1997) to determine
whole-brain patterns of activity correlated with seed regions that
showed similar increases of activity across the memory conditions
(Burianova and Grady, 2007). We hypothesized that autobiograph-
ical, “laboratory” episodic, and semantic retrieval would recruit a
large-scale functional network that underlies the general processes of
memory retrieval, such as top-down attentional control, response
monitoring, integration of contextual information, working memory
manipulation of to-be-retrieved information, and processing of
semantic representations.
Methods
Participants
Twelve right-handed, healthy young participants (mean age = 27
years; range = 21–37 years; 3 males), with at least 16 years of
education, took part in the study. All participants signed an informed
consent that was approved by ethics boards at Baycrest and
Sunnybrook Health Science Centre.
Stimuli
Experimental stimuli
Fifty colour and black and white photographs depicting general,
everyday events (e.g., driving or camping), as well as one-time but
highly publicized occurrences (e.g., the 9/11 attack on the World
Trade Center) were used as visual cues for the experimental retrieval
conditions.
867
Control stimuli
Five photographs were selected from the set of 50 described above
and scrambled using a Matlab script. This ensured that the visual
stimulus was rendered meaningless.
Procedure
The study consisted of one control and three memory retrieval
conditions during fMRI scanning. Four 14-min runs of 50 trials each
were presented to the participants in a counterbalanced order. Trials
were randomized within each run. In each trial, an experimental or
control stimulus was shown for 4 s. Each experimental stimulus was
shown three times during the experiment, but never in sequence or in
the same scanning run. Participants were asked to pay attention to the
photograph, so that they could successfully answer a subsequently
presented question that pertained to the stimulus. After the 4-s
presentation of each picture, a question appeared on the screen with
three possible answers.
Participants had 10 s to respond by pressing 1, 2, or 3 on a number
pad. Note that accuracy of memory retrieval was emphasized over
speed, and the participants were instructed not to guess. The response
period was chosen to provide sufficient time for autobiographical
memory retrieval. According to recent electrophysiological evidence,
the range of retrieval times for autobiographical memory is between 3
and 9 s, with an average time of 5 s (Conway et al., 2003). After the 10
second response period there was a 1-s inter-trial interval, followed
by the next trial. The three memory conditions were as follows:
1. Autobiographical condition, in which the stimulus was followed by
a cue designed to elicit a personal memory (e.g., “Think of the last
time you went camping”). Participants were asked to relive the
memory as vividly as possible and subsequently rate the memory
according to its vividness (1 = “very vivid,” 2 = “somewhat vivid,”
3 = “not vivid at all”).
2. Episodic condition, in which the stimulus was followed by a
question about the photograph itself (e.g., “In the picture, which
you have just seen, what is the colour of the tent?”). Participants
chose from three answers presented to them (1 or 2 being correct,
3 = I don't know). To ensure that this condition did not engage only
working or short-term memory, we varied the degree of difficulty
of retrieved contextual information; hence, the participants were
unaware of which piece of information about the stimulus they
would be asked to retrieve. In addition, the presentation of the
three experimental conditions was randomized and the temporal
lag between subsequent presentations of the same visual stimulus
was at least 14 min; hence, our intent was that participants would
need to engage episodic memory retrieval from long-term memory
storage about the perceptual details of the stimuli, and not solely
working memory processes.
3. Semantic condition, in which the stimulus was followed by a
factual type of question (e.g., “Are there more than 100 camping
grounds in Algonquin Park?”). Responses were made in the same
fashion as in the episodic condition.
In the control condition, the presentation of a scrambled
photograph was followed by an arbitrary instruction that was
unrelated to the stimulus itself (e.g., “Press a key that corresponds
to the letter ‘C’”). As in the experimental conditions, responses were
made by pressing 1, 2, or 3 on a keypad, and the correct key was either
1 or 2. Reaction times for each button press were recorded across all
conditions. These behavioural results have been reported elsewhere
(Burianova and Grady, 2007).
A post-scan interview was administered immediately after the
scan session. Participants viewed the 50 photographs again and were
asked to describe the autobiographical memory that had been
retrieved during the scan in as much detail as possible. Temporal
and spatial information as well as the content of the event and
868 H. Burianova et al. / NeuroImage 49 (2010) 865–874
participant's emotion at the time of its occurrence were recorded by
the experimenter, to ensure that each autobiographical memory was
accompanied by a vivid recollection of a particular episode.
fMRI data acquisition
Anatomical and functional images were collected using a 3T GE
scanner with a standard head coil. A standard, high resolution, T1-
weighted volumetric anatomical MRI (124 axial slices, 1.4 mm thick,
FOV = 22 cm, acquisition matrix = 256 × 256 × 124, TR = 35 ms,
TE = 6 ms, flip angle = 35°) was acquired for each participant. Brain
activation was assessed using the blood oxygenation level-dependent
(BOLD) effect (Ogawa et al., 1990) with optimal contrast. For functional
imaging, 26 axial slices of 5 mm thickness were obtained, utilizing a
T2⁎-weighted pulse sequence with spiral in-out readout (TR =
2000 ms, TE = 30 ms, FOV = 20, acquisition matrix = 64 × 64 × 26, flip
angle = 80°).
Visual stimuli were presented using fMRI-compatible goggles
(Avotec, Inc.) mounted on the head coil. Responses were collected
with the Rowland USB Response Box (RURB).
fMRI data preprocessing
Images were reconstructed and motion-corrected utilizing the
Analysis of Functional Neuroimages (AFNI; Cox, 1996). The images
were spatially co-registered to correct for head motion of the
participants by using a 3D Fourier transform interpolation. The peak
range of head motion did not exceed 1.2 mm across all participants. To
enable group comparisons, each brain scan was spatially normalized,
i.e., scaled and warped to match a standard template (the Montreal
Neurological Institute [MNI] spiral template) utilizing Statistical
Parametric Mapping (SPM99) software. The warping of the brain
surface was achieved via a linear transformation with sinc interpo-
lation (i.e., a signal resampling method designed to minimize aliasing
in the signal). Lastly, the images were smoothed with a 6 mm
Gaussian filter (in SPM), which, acting as a low pass filter, makes the
data less noisy by reducing the images' high-frequency components.
The voxel size, after preprocessing, was 4 × 4 × 4 mm.
Seed voxel PLS
In the seed PLS analysis, we included those trials for the semantic
and episodic conditions for which participants made a correct
response, and all “very vivid” and “somewhat vivid” trials for the
autobiographical condition. Seed PLS is a multivariate statistical
method utilized in the investigation of the relation of activity in a
selected brain region or regions (i.e., a seed voxel) and activity in the
rest of the brain across the task conditions (Della-Maggiore et al.,
2000; Schreurs et al., 1997; McIntosh, 1999; McIntosh et al., 1997). In
other words, seed PLS analysis examines task-related functional
connectivity. The selection of the seed voxel(s) can be either data-
driven (i.e., determined by previous analyses of the data) or
hypothesis-driven (i.e., determined by theoretical assumptions), or
both. In our study, the selection of the seed voxels used in the seed PLS
analysis was data-driven. In a previous study (Burianova and Grady,
2007), we identified eight brain regions whose activity was
significantly increased across all three memory conditions, thus
showing activity common to the conditions. To determine whether
these regions are also a part of the same functional network, we
entered all eight regions into a seed PLS analysis. The analysis revealed
a connectivity pattern across the three memory conditions, but not all
regions were reliably correlated with this pattern. Therefore, a
subsequent analysis was carried out, using the three seed regions
that covaried most strongly with the rest of the brain across the three
memory conditions—the left hippocampus, right caudate nucleus, and
left lingual gyrus (see Table 1 for the coordinates).
Table 1
Seed voxel regions.
Region Hem BA Talairach coordinates Ratio
x y z
Caudate nucleus R n/a 12 15 −4 6.2
Lingual gyrus L 18 −4 −70 3 4.9
Hippocampus L n/a −28 −20 −16 6.9
Abbreviations: Hem = hemisphere; BA = Brodmann's area; R = right; L = left;
Ratio = salience/SE ratio from the bootstrap analysis; x coordinate = right/left; y
coordinate = anterior/posterior; z coordinate = superior/inferior.
This analytical procedure for seed PLS was threefold: firstly, the
BOLD values from the selected seed(s) were extracted (i.e., from the
peak voxels identified in our previous study), across 8 timepoints after
each presentation of the question cue to capture activity during the
retrieval phase of the trial. The activity for each seed was averaged
across the peak and adjacent timepoints, and then this average
measure of seed activity was correlated with activity in all other brain
voxels, across all participants, within each condition. Secondly, these
correlations were combined into a matrix and decomposed with
singular value decomposition (SVD), resulting in a set of latent
variables (LVs; mutually orthogonal variables). Each LV consists of a
singular image (i.e., “brain LV,” or the pattern of brain regions that
covary in activity with the seed voxel), a singular profile (i.e., “seed LV,”
or the pattern of covariance of the seed voxel and the rest of the brain
across the experimental conditions), and a singular value (i.e., the
amount of covariance accounted for by each LV). Finally, the
significance for each LV is determined by using a permutation test
(McIntosh et al., 1996), which involves a random reordering of the
data matrix and calculation of a new set of LVs for each reordering. The
singular value of each newly permuted LV is compared to the singular
value of the original LV, yielding a probability of the number of
occurrences that the permuted values exceed the original value. Five
hundred permutations were conducted. Because this study used an
event-related design, the PLS analysis provided a set of correlated
regions (i.e., a map of areas correlated with the seeds) for each of the
eight TRs in the analysis. For each TR, a “brain score” was calculated for
each participant that is an index of how strongly that participant
shows the particular pattern of brain activity identified for that TR. The
brain scores can be used to examine differences in brain activity across
conditions, because greater activity in brain areas with positive (or
negative) weights on a latent variable will yield positive (or negative)
mean scores for a given condition. We calculated the correlation
between the brain scores from each significant LV and the seed BOLD
values to assess the relation between the whole-brain pattern and
activity in the three reference regions. In addition to the permutation
test, a second and independent step is to determine the reliability of
the saliences (or weights) for the brain voxels characterizing each
pattern identified by the LVs. To do this, all saliences for each TR were
submitted to a bootstrap estimation of the standard errors (Efron and
Tibshirani, 1985), randomly resampling participants, with replace-
ment, and computing the standard error of the saliences after 100
bootstrap samples. Peak voxels with a salience/SE ratio N3.0 were
considered to be reliable, as this approximates p b 0.005 (Sampson et
al., 1989). Because PLS uses images in the format developed by the
Montreal Neurological Institute (MNI), all coordinates resulting from
the PLS analyses were converted from MNI space to Talairach
coordinates using the algorithm developed by Brett and colleagues
(www.mrc-cbu.cam.ac.uk/Imaging/Common/mnispance.shtml).
Correlation analysis
The seed PLS, using the three seeds, resulted in a set of 18 regions
whose activity was reliably and strongly correlated with all three, and
this set of regions constituted the putative common network. To
 H. Burianova et al. / NeuroImage 49 (2010) 865–874 869

Table 2 correlated with all three seed regions (the left hippocampus, left
Correlations with seed activity. lingual gyrus, and right caudate nucleus) during the retrieval of
Region Hem BA Talairach coordinates Ratio Cluster autobiographical, episodic, and semantic memories (see Fig. 1). Positive
correlations with the three seed regions were found in temporal cortex
x y z
(bilaterally in the middle temporal gyrus and superior temporal gyrus),
Positive correlations
frontal cortex (bilateral inferior frontal gyrus, medial frontal gyrus, and
Inferior FG L 47 −36 38 −9 6.8 50
R 47 48 23 −11 5.6 29 left anterior cingulate gyrus), as well as in the left temporoparietal
Medial FG L 10 −4 50 −6 6.9 25 junction and posterior cingulate gyrus. Negative correlations with the
Anterior CG L 24/32 −8 35 9 6.6 30 seed regions were found in the left middle occipital gyrus, right
Superior TG L 22 −55 −53 21 5.9 35 thalamus, bilateral precuneus, bilateral fusiform gyrus, and bilateral
Middle TG L 21 −48 −20 −2 6.5 74
R 21 48 −20 −2 7.7 83
supramarginal gyrus (see Table 2 for a summary). These patterns of
Temporal pole R 22 51 8 −4 7.1 70 correlation were found across all three memory conditions.
Inferior PL (TPJ) L 40 −63 −49 32 7.0 25
Posterior CG 23/31 0 −61 21 7.3 74 Correlation analysis
Negative correlations
Middle OG L 19 −40 −81 15 −5.4 29 The seed PLS analysis identified a set of regions correlated with the
Precuneus L 7 −8 −79 45 −7.2 44 seeds across all three memory conditions. To assess further whether
R 7 12 −83 45 −6.9 95 this set of regions represents a common memory retrieval network,
Thalamus R n/a 4 −15 15 −7.5 18 we determined if the correlations among all the nodes of this putative
Inferior TG L 37 −55 −51 −8 −6.5 52
Fusiform gyrus R 20 40 −28 −19 −8.6 80
network were statistically equivalent across the tasks, as one would
Inferior PL (SMG) L 40 −36 −52 39 −9.8 100 expect if the network operates in a similar fashion regardless of the
R 40 32 −53 36 −9.3 34 task demands. Fig. 2 shows three correlation matrices representing
Abbreviations: Hem = hemisphere; BA = Brodmann's area; R = right; L = left; the 3 seeds and the 18 regions that showed correlated activity with
Ratio = salience/SE ratio from the bootstrap analysis; Cluster = size of each cluster in the seeds, both positive and negative. Each matrix shows the visual
number of voxels; FG = frontal gyrus; CG = cingulate gyrus; TG = temporal gyrus; representation of interregional correlations of activity among the 21
OG = occipital gyrus; PL = parietal lobule; TPJ = temporoparietal junction; regions, within each memory condition. No significant differences
SMG = supramarginal gyrus; x coordinate = right/left; y coordinate = anterior/
posterior; z coordinate = superior/inferior.
(p N 0.05) were found in the overall interregional correlation strengths
across the three memory conditions. The correlation matrices indicate
that during all memory conditions, most of the regions that positively
specifically examine the intercorrelations among these regions, we correlated with the seeds were also correlated positively with one
extracted the BOLD signal from them, i.e., from the peak voxel in each another (denoted in lighter shades of gray), but negatively with
cluster (see Table 2 for peak coordinates), and averaged the activity at regions that show negative correlations with the seeds (denoted in
the timepoint corresponding to the strongest correlation with the darker shades). Similarly, most of the regions with negative seed
seeds and adjacent timepoints. We then calculated interregional correlations correlated positively with each other, but negatively with
correlations within conditions (creating three 21 × 21 correlation the regions with positive seed correlations. Despite some apparent
matrices) and compared these correlation patterns across conditions. interregional differences, there are obvious clusters of strong positive
We compared the correlation patterns across the conditions by and negative correlations among the voxels that are consistent across
calculating the squared differences in correlations (for each cell of the the three memory conditions. As a whole, the strength of the overall
matrix) between conditions and summing them to obtain a single interregional correlations did not differ across the conditions,
value for the overall difference in correlations between conditions. consistent with the idea of a common functional memory network.
The statistical significance of this difference was assessed using a
permutation test on the sum of squared differences (McIntosh et al., Discussion
1996), which involved a random reordering of the data matrix and
calculation of a new set of values for each reordering. The purpose of this study was to identify a functional network that
is common to autobiographical, episodic, and semantic retrieval. The
Results results of the seed PLS analysis yielded a large-scale network of brain
regions that were functionally connected to the left hippocampus,
Behavioural performance right caudate nucleus, and left lingual gyrus in all memory retrieval
conditions. The inferior frontal gyri, medial frontal gyrus, anterior and
Behavioural performance was assessed by comparing the means of posterior cingulate gyri, left temporoparietal junction, and a number
the response times across the four conditions (correct trials only), of temporal areas (bilateral middle temporal gyrus, superior temporal
using a repeated-measures ANOVA. The effect of condition was gyrus, and right temporal pole) positively correlated with the seed
significant, F(3,33) = 73.1, p b 0.001. Pairwise t-tests with Bonferroni regions, whereas the left middle occipital gyrus, bilateral precuneus,
corrections for multiple comparisons showed that the response times right thalamus, left inferior temporal gyrus, right fusiform gyrus, and
for autobiographical retrieval (M = 6989 ms, SD = 1478) differed bilateral inferior parietal lobule negatively correlated with the seed
significantly from that for the control task (M = 1925 ms, SD = 728) regions. These results suggest that these areas, as a whole, comprise a
and episodic retrieval (M = 4640 ms, SD = 1150, both at p b 0.01). The common functional network that subserves the general processes of
difference in reaction time (RT) for autobiographical retrieval and declarative memory retrieval. We propose that these processes
semantic retrieval (M = 5858 ms, SD = 1366) approached significance include a multitude of higher-cognitive functions, for instance,
(p = .06). working memory, selective attention, error monitoring, response
verification, and comprehension of concept representations. We
Seed PLS conclude from these results that, together, these cognitive processes
and their integration are essential to what is defined as ‘declarative
The first latent variable yielded by the three-seed PLS analysis memory retrieval.’
accounted for the largest amount of covariance in the data (32%; The three seed regions selected for the functional connectivity
p b 0.002), delineating a group of brain regions whose activity analysis have been previously identified as important for memory
870 H. Burianova et al. / NeuroImage 49 (2010) 865–874

Fig. 1. Seed PLS results: common functional network. (a) A pattern of correlated activity at 6–8 s after retrieval onset is shown. (b) A pattern of correlated activity at 10–12 s after
retrieval onset is shown. (c) Correlations of activity in the three seeds with the brain scores (summary measures of whole-brain activity in each subject per condition) are plotted to
show how activity in the seeds correlates with activity in the entire network. The error bars represent confidence intervals based on the bootstrap. (d) Activity in the caudate nucleus
at 2–3 s after retrieval onset is shown. Yellow/red = positive correlations with the seeds; blue = negative correlations with the seeds.

processing (e.g., Burianova and Grady, 2007). The hippocampus has
been implicated as a critical component of declarative retrieval
processes (Cabeza et al., 2004; Eldridge et al., 2000; Prince et al., 2005)
and relational memory (e.g., memory for the relations between items
and context [e.g., Davachi and Wagner, 2002], or between objects and
features of a scene [e.g., Ryan and Cohen, 2004]). The hippocampus
also may play a role in non-declarative processes, such as working
memory and object organization (Seeck et al., 1995) and non-
mnemonic processes, such as local feature extraction in form
perception (Barense et al., 2005; Beason-Held et al., 1998) and visual
discrimination of scenes (Davies et al., 2004). The left lingual gyrus
has been linked to working memory maintenance of visuospatial
information (Ragland et al., 2002), imagery (Kosslyn et al., 1993;
Mazard et al., 2005), and crossmodal attention (Ferber et al., 2007).
The caudate nucleus also was found to be involved in learning and
memory, particularly in regard to feedback processing and the ability
to shift a cognitive set in response to the environment (Packard and
Knowlton, 2002).
The three seed regions were found to positively covary with a
number of frontal, temporal, and parietal areas. These areas of
functional connectivity broadly overlap with the common memory-
related brain regions, which were found in our previous analysis
(Burianova and Grady, 2007), although the exact locations are not
identical. The inferior frontal gyrus has been implicated in declarative
and working memory retrieval (Nyberg et al., 2002), as well as in
response inhibition and selection control (Aron et al., 2004; Brass et
al., 2005; Liddle et al., 2001), and top-down attentional control
(Banich et al., 2000; Dove et al., 2008). The medial prefrontal areas are
involved in social functions and self-referential processes in both
semantic and episodic memory retrieval (Addis et al., 2004a,b; Gilboa
et al., 2004; Levine et al., 2004). The functional connectivity of these
frontal areas with the three seed regions suggests involvement of the
frontostriatal and hippocampo-frontal pathways. The frontrostriatal
pathway has been implicated in abstract reasoning (Melrose et al.,
2007), working memory (Ashby et al., 2005; Gazzaley et al., 2004),
and internal object representations (Kraut et al., 2002), as well as in
attentional control and cognitive planning and execution of a set-shift
(Monchi et al., 2006), due to its predominant dopamine dependency
(Chudasama and Robbins, 2006) and dopamine–glutamate interac-
tions (Smith et al., 2004). The hippocampo-frontal pathway, involving
the left hippocampus, has been linked to the retrieval of contextual
details (Svoboda et al., 2006), despite some researchers' arguing its
sole involvement in autobiographical memory retrieval (e.g., Addis et
al., 2007). The common prefrontal link of the frontostriatal and
hippocampo-frontal pathways allows for an indirect effect of the
caudate nucleus on the hippocampus and vice versa. Some research-
ers speculate that the hippocampus and caudate nucleus functionally
interact to jointly mediate behavioural output during performance
(Dagher et al., 2001; Packard and Knowlton, 2002). We propose that
the frontal nodes of the common retrieval network subserve top-
down attentional, inhibitory, and monitoring functions, as well as
working memory manipulation and maintenance of information
necessary for a successful declarative recollection of memories that
relate to the self and others.
The middle and superior temporal gyri were involved in our
common network, and have been linked to the processing of personal
 H. Burianova et al. / NeuroImage 49 (2010) 865–874 871

Fig. 2. Correlations among peak voxels of the common functional network. The three correlation matrices show similarities in regional interrelations across the three memory
conditions. Correlation values are indicated by shades of gray (positive correlations are denoted in lighter shades; negative correlations are denoted in darker shades). Values on the
vertical and horizontal axes correspond to the region numbers in the attached legend. The matrix is symmetrical about the main diagonal, which corresponds to perfect correlation
(+1) of each voxel with itself. STG = superior temporal gyrus; CN = caudate nucleus; IPL = inferior parietal lobule; IFG = inferior frontal gyrus; pCG = posterior cingulate gyrus;
aCG = anterior cingulate gyrus; LG = lingual gyrus; MTG = middle temporal gyrus; med FG = medial frontal gyrus; HIPP = hippocampus; MOG = middle occipital gyrus;
PCU = precuneus; TH = thalamus; ITG = inferior temporal gyrus.

and general semantic representations (e.g., Martin and Chao, 2001),
which are essential in the retrieval of all declarative memory. Martin
and Chao (2001) further note a temporo-frontal pathway, connecting
the middle and superior temporal areas with the inferior prefrontal
cortex, enabling the retrieval, monitoring, and manipulation of
semantic representations. Levine et al. (1999) found impaired
autonoetic processing (due, hypothetically, to deficits in self-regula-
tion) in patient ML, whose traumatic brain injury led to a
disconnection of the temporal and frontal lobes, in the right
hemisphere. The functional relevance of the temporopolar area is
much less clear but its functional connectivity with the hippocampus,
middle and superior temporal gyri, and the temporoparietal junction
suggests its involvement in multimodal perceptual analysis (Olson et
al., 2007), as the temporal pole is speculated to be a convergence area,
which integrates diverse streams of information into a unified whole
(Markowitsch et al., 1985). Other researchers have suggested that
both the temporal pole and the left temporoparietal junction are
critical in the encoding of personal memories (Nakamura and Kubota,
1996), multisensory processing of body and self (Arzy et al., 2006),
retrieval of theory-of-mind information (i.e., when comprehending
someone else's state of mind; Arzy et al., 2006; Moriguchi et al., 2006),
and conceptual knowledge (Graham et al., 2003). Our finding that
these temporal and parietal regions are nodes of the common
retrieval network suggests that these areas participate in the
processing of necessary semantic representations, as well as the
convergence of relevant semantic, perceptual, and others' state of
mind information of which declarative memories are composed.
The anterior and posterior cingulate gyri are known to be
bidirectionally connected to one another via the cingulum bundle
(Goldman-Rakic, 1988; Vogt et al., 1979) and indirectly via the medial
temporal lobes (Morris et al., 1999), with functional connections to
the temporal, frontal, and parietal lobes. Thus, they are speculated to
be involved in a variety of cognitive and emotional processes (e.g.,
Bush et al., 1998; Critchley et al., 2003), including self-referential
872 H. Burianova et al. / NeuroImage 49 (2010) 865–874
(Gusnard, 2005; Gusnard et al., 2001) and visuospatial processing
(e.g., Rosenbaum et al., 2004). Although the anterior part of the
cingulate gyrus is often linked to uniquely autobiographical processes
(Svoboda et al., 2006), other researchers found it active in both
episodic and semantic processes (e.g., Mummery et al., 1996). Johnson
et al. (2006) linked both the anterior and posterior cingulate gyri to
self-reflection, albeit linking the anterior cingulate cortex to instru-
mental self-reflection (i.e., directed towards the inner self) and the
posterior cingulate cortex to experiential self-reflection (i.e., directed
towards the self as it relates, externally, to others). The involvement of
the anterior and posterior cingulate gyri in the common retrieval
network emphasizes the critical role of intrinsically driven and self-
related processes in declarative memory search and retrieval. Thus, it
should come as no surprise that these regions overlap with the
‘default-mode’ regions whose activity decreases during demanding
external tasks, but increases during self-referential processing and
monitoring of the internal environment (e.g., Gusnard, 2005). The
anterior and posterior cingulate gyri are two frequently delineated
nodes of this self-referential default-mode network (e.g., Fox et al.,
2005; Greicius and Menon, 2004; Gusnard et al., 2001; Toro et al.,
2008).
Finally, the connectivity analysis yielded a number of functionally
connected brain areas that negatively correlated with the left
hippocampus, lingual gyrus, and right caudate nucleus, yet positively
correlated with one another. These areas included the left middle
occipital gyrus, bilateral precuneus, right thalamus, left inferior
temporal gyrus, right fusiform gyrus, and bilateral inferior parietal
lobule. Given the similarity between these regions and attentional
networks proposed by Corbetta et al. (2000, 2008), these negatively
correlating regions are likely involved in attention to external stimuli.
In a recent study, Fu et al. (2005) found a network of posterior brain
areas, including the middle occipital gyrus, precuneus, fusiform gyrus,
and inferior parietal lobes, that was involved in externally driven early
visuospatial attentional modulation, as well as in later perceptual
feedback to the primary visual areas. In the paradigm used here, the
processing of memory search is internally driven and our analysis
focused only on the period of retrieval, not on the period of cue
presentation. Thus, when the common network is recruited for this
internal process (i.e., an increase in activity), activity in the externally
driven occipito-temporo-parietal network is reduced, or maybe even
suppressed (i.e., a decrease in activity). It is likely that the externally
driven network would be more active if memory were more directly
cued by an external stimulus, consistent with the idea of Ciaramelli et
al. (2008) that different parts of the parietal cortex mediate attention
to retrieval cues in memory search.
In conclusion, the results of this study yielded a large-scale
functional network of frontal, temporal, and parietal areas, as well as
the anterior and posterior cingulate gyri, in line with the unitary
systems view that suggests a single declarative memory system
(Baddley, 1984; Friston, 2002; Kihlstrom, 1984; McIntosh, 1999; Rajah
and McIntosh, 2005; Roediger, 1984). The functional connections
within this network did not significantly differ across the memory
conditions, indicating its importance in all types of declarative
retrieval. This neural overlap of autobiographical, “laboratory”
episodic, and semantic retrieval suggests that all declarative memory
retrieval engages a set of functional processes, mediated by the use of
this common network, and provides further support for the notion of a
unitary memory system. One implication of this unitary system is that
no declarative memory retrieval is ever purely “semantic” or
“autobiographical,” for example, but necessarily involves overlapping
processes and multiple types of content, both contextual and context-
free. The regions that we found to be part of the common network
suggest that some of these overlapping cognitive processes that are
involved in declarative memory are likely to include top-down
attentional, inhibitory, and monitoring processes, working memory
manipulation, maintenance of information, and convergence of
semantic and self-referential information. Activity in this network
during memory retrieval may be facilitated by down-regulation of an
occipito-temporo-parietal network of posterior brain areas, which
supports attentional modulation in response to external stimuli.
Acknowledgments
We thank the staff at Sunnybrook Health Science Centre for their
assistance in this experiment. This work was funded by the Canadian
Institutes of Health Research (grant MOP 14036). C.L. Grady is also
supported by the Canada Research Chairs program, the Ontario
Research Fund, and the Canadian Foundation for Innovation.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.neuroimage.2009.08.066.
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