Neuropsychologia 143 (2020) 107495

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Neuropsychologia
journal homepage: http://www.elsevier.com/locate/neuropsychologia

Neural correlates of successful emotional episodic encoding and retrieval:

An SDM meta-analysis of neuroimaging studies
Kristina Dahlgren , Charles Ferris , Stephan Hamann *
Department of Psychology, Emory University, 36 Eagle Row, Atlanta, GA, 30322, USA

A R T I C L E I N F O A B S T R A C T

Keywords: Episodic memory for emotional events is typically enhanced and engages additional brain mechanisms relative to
Neuroimaging episodic memory for neutral events. Many functional magnetic resonance imaging (fMRI) studies have probed
Episodic memory the neural basis of this emotional enhancement effect on encoding processes, while relatively fewer studies have
Encoding
examined retrieval. Neuroimaging meta-analysis methods can summarize the brain regions associated with
Retrieval
Emotion
emotional episodic memory that are consistently activated across multiple studies. A previous ALE (Activation
Amygdala Likelihood Estimation) meta-analysis identified consistent activations associated with successful encoding of
episodic emotional memory in the amygdala, hippocampus, and in multiple neocortical regions (Murty et al.,
2010). However, since that study, meta-analysis methods have improved, and many new relevant neuroimaging
studies have been published. Moreover, although qualitative reviews have summarized brain activations related
to the successful retrieval of emotional episodic memory, no corresponding quantitative meta-analyses have yet
been reported. Here we conducted neuroimaging meta-analyses of successful emotional memory encoding and
rretrieval using Seed-based d Mapping (SDM). Relevant neuroimaging studies reporting whole-brain fMRI cor­
relates of successful encoding and retrieval of emotional episodic memory were selected for analysis. For suc­
cessful emotional memory encoding, SDM activations were found bilaterally in the medial temporal lobe
(amygdala, hippocampus, entorhinal cortex, perirhinal cortex, and parahippocampal cortex), bilaterally in visual
processing regions (middle temporal, gyrus, fusiform gyrus and occipital cortex) and bilaterally in the temporal
pole, orbitofrontal cortex, insula, putamen, and the inferior and middle temporal gyri. In contrast to the prior
meta-analysis, SDM activations were not observed in the inferior frontal gyrus or in parietal regions. For suc­
cessful emotional episodic memory retrieval, SDM activations were observed in the medial temporal lobe
(bilateral amygdala, left hippocampus, and left entorhinal cortex and perirhinal cortex), visual processing re­
gions (bilateral occipital cortex and right middle temporal gyrus), prefrontal cortex (bilateral orbitofrontal
cortex, bilateral inferior frontal gyrus, bilateral precentral gyrus, left middle frontal gyrus, right frontal pole) and
other regions in the left hemisphere including the temporal pole, insula, putamen, angular gyrus, and parietal
opercular cortex. Considerable overlap was observed between the encoding and retrieval meta-analysis maps in
the medial temporal lobe (bilateral amygdala, left hippocampus, entorhinal, and perirhinal cortex), visual pro­
cessing regions (bilateral occipital cortex, right middle temporal gyrus), and other regions including the left
orbitofrontal cortex, left insula, left putamen, left pallidum, and left temporal pole. The current findings add to
current understanding of the role of the amygdala, hippocampus, and neocortical regions in the successful
encoding and retrieval of emotional episodic memory, clarify and provide an important summary of the current
literature in this area, and have implications for current theories of emotional episodic memory encoding and
retrieval.

1. Introduction of past events that are associated with a specific time and place, as
distinct from semantic memory (memory for factual knowledge)
Episodic memory, as defined by Tulving (1983, 2002) refers to a (Tulving, 1985). The definition of episodic memory has subsequently
neurocognitive memory system that enables the conscious remembering been elaborated and expanded to include key psychological components

* Corresponding author.
E-mail address: shamann@emory.edu (S. Hamann).

https://doi.org/10.1016/j.neuropsychologia.2020.107495
Received 24 October 2019; Received in revised form 7 May 2020; Accepted 8 May 2020
Available online 13 May 2020
0028-3932/© 2020 Elsevier Ltd. All rights reserved.
K. Dahlgren et al.
such as autonoetic awareness (i.e., awareness during memory retrieval
that the memory is from a time in one’s own past) and characterization
of the brain regions and processes associated with episodic memory
encoding and retrieval (Tulving, 2002). The critical importance of
episodic memory is vividly illustrated by the severe deficits exhibited by
patients with amnesia (Eichenbaum et al., 2007; Hamann and Squire,
1995; Squire, 2004; Squire et al., 2007).
The brain basis for episodic memory has been investigated using a
wide range of neuroscience methods including neuropsychological le­
sions, electrophysiological methods such as event related potentials
(ERP) and magnetoencephalography (MEG), and structural and func­
tional neuroimaging methods such as positron emission tomography
(PET) and functional magnetic resonance imaging (fMRI) (Addis et al.,
2015; Moscovitch et al., 2016; Tulving and Craik, 2005). Much of cur­
rent knowledge of the brain basis of episodic memory in humans is based
on the findings of event-related fMRI studies that investigated the neural
correlates of successful encoding and retrieval. For example, to identify
activity at encoding related to successful subsequent memory, the sub­
sequent memory paradigm (Paller and Wagner, 2002) assesses
event-related activity that is related to successful retrieval on a subse­
quent test (encoding success activity; ESA) by back-sorting items pre­
sented at encoding into those that are subsequently remembered (hits)
vs. those that are forgotten (misses) and taking the difference (activity
for subsequently remembered minus forgotten items). This procedure
yields a statistical map reflecting brain areas where event-related
(transient) activity predicts successful encoding. A similar procedure
can be used to identify retrieval success activity (RSA) by contrasting
item-specific fMRI activity for successful vs. unsuccessful memory
retrieval trials (e.g., recognition hits minus misses). These contrasts are
commonly referred to as difference in memory contrasts or DM con­
trasts. Qualitative reviews and quantitative meta-analyses have sum­
marized the brain regions that are most commonly recruited during
successful encoding and retrieval of episodic memory. In addition to the
hippocampus and other medial temporal lobe regions, successful
encoding and retrieval recruit multiple prefrontal, parietal, and occipital
regions (Benoit and Schacter, 2015; Habib et al., 2003; McDermott et al.,
2009; Spaniol et al., 2009).
Emotion can strongly influence multiple aspects of cognition,
including episodic memory encoding and retrieval. One of the most
salient and extensively studied effects of emotion is the emotional
enhancement of memory effect: episodic memory for emotionally arousing
stimuli and events is typically stronger, more resistant to forgetting, and
more vivid relative to memory for comparable neutral stimuli and events
(Hamann, 2001; Kensinger, 2004; Kensinger and Schacter, 2008a; LaBar
and Cabeza, 2006; Phelps and Sharot, 2008). The memory-enhancing
effects of emotional arousal can also carry over to enhance memory
for neutral stimuli experienced either a short time before or after
emotionally arousing events (Dunsmoor et al., 2015; Tambini et al.,
2010). Although episodic memory associated with emotion shares many
broad similarities with ordinary, non-emotional episodic memory,
considerable evidence from lesion studies and neuroimaging studies
supports the view that emotional episodic memory involves special
brain mechanisms that can enhance memory (Hamann, 2001; LaBar and
Cabeza, 2006; Phelps, 2004). This emotional enhancement occurs for
both positive (pleasant) and negative (unpleasant) episodic memory
(Bowen et al., 2018; Dolcos et al., 2004; Hamann, 2009).
Although there are many theoretical accounts of emotional episodic
memory effects, most theoretical accounts distinguish between two
main mechanisms of emotional enhancement of memory: an amygdala-
mediated direct route in which the amygdala has a direct enhancing role
and an indirect route that involves top-down enhancement of memory via
primarily prefrontally mediated mechanisms. In the amygdala-mediated
route, the amygdala modulates and enhances activity related to memory
encoding in the medial temporal lobe and in perceptual regions such as
visual cortex (Bowen et al., 2018; Kark and Kensinger, 2019; LaBar and
Cabeza, 2006; Todd et al., 2012). This amygdala-mediated enhancing
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Neuropsychologia 143 (2020) 107495
influence of emotion also can continue after encoding to affect consol­
idation processes (Cahill and McGaugh, 1998; Hamann, 2001;
McGaugh, 2004 Tambini et al., 2010). By contrast, the indirect, pre­
frontally mediated route involves top-down interactions that modulate
activity in regions mediating attention, semantic elaboration, and other
cognitive processes known to enhance episodic memory (Dolcos, Kat­
sumi, Denkova, Weymar and Dolcos, 2017a; Dolcos et al., 2017b; Ken­
singer and Corkin, 2004). The relative contribution of each route to
memory enhancement appears to depend on many factors including the
intensity of emotional arousal at encoding, the emotional valence of the
stimuli, and whether attention is divided at encoding (Bowen et al.,
2018; Dolcos et al., 2017a,b; Talmi, 2013).
A large number of neuroimaging studies have investigated emotional
episodic memory encoding and retrieval in recent years, providing
important insights into the brain basis of emotional episodic memory
(Dolcos et al., 2017a,b; Hamann, 2001; Kensinger and Schacter, 2008a;
LaBar and Cabeza, 2006). Synthesizing and integrating the findings of
these studies has been challenging for many reasons, however. Differ­
ences across studies in tasks, stimuli, and generally low statistical power
for individual studies all complicate efforts to summarize findings.
While qualitative, narrative reviews can be informative, quantitative
meta-analyses allow the results of multiple studies to be pooled and
analyzed using a rigorous statistical framework that can identify regions
of consistent activations associated with a construct such as emotional
episodic memory (Albajes-Eizagirre and Radua, 2018; Eickhoff et al.,
2012; Müller et al., 2018; Radua and Mataix-Cols, 2012; Wager et al.,
2007).
Coordinate based meta-analysis (CBMA) methods such as Activation
Likelihood Estimation (ALE) and Seed-based d Mapping (SDM), among
others, are widely used quantitative neuroimaging meta-analytic
methods (Albajes-Eizagirre and Radua, 2018; Costafreda et al., 2009;
Eickhoff et al., 2009; Eickhoff et al., 2012; 2016; Kang et al., 2011; Kang
et al., 2014; Laird et al., 2005;Montagna et al., 2018; Radua et al., 2012,
2014; Radua and Mataix-Cols, 2009, 2012; Tench et al., 2017; Turkel­
taub et al., 2012; Wager et al., 2007; Yue et al., 2012). These CBMA
methods perform statistical tests on activation foci coordinates reported
in individual neuroimaging studies, thereby identifying brain regions
that are consistently activated across studies and producing a
whole-brain summary of activations associated with a construct of in­
terest. These quantitative meta-analytic approaches have many advan­
tages over qualitative reviews and provide a relatively unbiased method
of synthesizing results that retains much of the spatial information of the
original neuroimaging studies.
Murty et al. (2010) conducted the first ALE meta-analysis identifying
the brain regions that are consistently activated across studies of suc­
cessful emotional episodic memory encoding. Their results were
generally in agreement with predictions based on the two main routes
for emotional memory enhancement, the direct amygdala-mediated
route and the indirect, prefrontally mediated route. Consistent with
the amygdala-mediated modulation route, they reported ALE clusters in
the bilateral amygdala, anterior hippocampus, the parahippocampal
gyrus, and parts of the ventral visual stream. In line with the prefrontally
mediated route, they also reported ALE clusters in several prefrontal and
parietal regions. This influential meta-analysis helped to summarize and
clarify the empirical support for theoretical accounts of emotional
episodic memory and has been widely cited. However, since this pre­
vious meta-analysis of successful emotional memory encoding (Murty
et al., 2010) was published, nearly ten years of new neuroimaging
studies examining emotional memory have been published and limita­
tions of the ALE methodology used by Murty et al. (2010) have subse­
quently been identified and resolved in newer meta-analytic methods.
Two critical problems have been identified in the ALE methodology
used by Murty et al. (2010). One important problem is that it tested for
convergence of findings (i.e., the probability that reported findings in
surrounding voxels are greater than chance compared to permutations
of random distributions of peaks) rather than testing against the null at
K. Dahlgren et al.
the voxel level (Albajes-Eizagirre and Radua, 2018; Laird et al., 2005).
This method of testing for convergence has been criticized as problem­
atic because it relies on assumptions of spatial independence of activa­
tion that are often violated in spatially correlated fMRI neuroimaging
data (e.g., local peaks within the same cluster or region are not randomly
distributed in the brain and peaks are more likely to be located in grey
matter rather than white matter or CSF) (Albajes-Eizagirre and Radua,
2018; Albajes-Eizagirre et al., 2019). Another important issue with the
previous ALE methodology is the use of the false discovery rate (FDR)
method to correct for multiple comparisons. Recent theoretical work has
established that FDR correction for multiple comparisons in ALE
meta-analyses relies on assumptions of spatial independence that are
violated in spatially correlated neuroimaging data containing clusters of
activation, with the net effect of not adequately controlling the false
positive rate and increasing the chance of spurious findings (Chumbley
and Friston, 2009; Eickhoff et al., 2012, 2016).
Seed-based d Mapping Permutation of Subject Images (SDM-PSI)
(https://www.sdmproject.com/), the method used in the current study,
has resolved these issues and added additional important features not
currently implemented in ALE (Albajes-Eizagirre et al., 2019; Eickhoff
et al., 2012, 2016). First, to address issues of spatial non-independence,
SDM incorporates information about differences in effect size and the
spatial correlations of different brain tissue types. Second, SDM conducts
permutation testing at the subject level that allows for voxel-wise tests of
statistical significance (Albajes-Eizagirre et al., 2019). These features
result in improved control of false positives and increased reliability
compared to ALE, especially when the number of studies included in the
meta-analysis is less than 35, as is the case for the current meta-analysis
(Bossier et al., 2018). Third, SDM uses voxel-wise significance testing
combined with threshold-free cluster enhancement (TFCE, a method
which simulates cluster-wise effects by enhancing voxel-wise statistical
values for voxels which are close together) to adequately control for
multiple comparisons while avoiding the use of arbitrary cluster size
thresholds (Albajes-Eizagirre et al., 2019; Smith and Nichols, 2009). A
major consequence of this statistical method is that it can detect sub­
stantially smaller regions of activation (as small as single activated
voxels), relative to cluster-based thresholding methods.
In light of these issues, there is a compelling rationale for updating
current meta-analytic knowledge regarding the brain correlates of
emotional episodic memory. Specifically, to address this key gap in the
literature, we conducted an SDM meta-analysis examining a signifi­
cantly larger set of fMRI studies of emotional memory encoding, using
the most recent SDM-PSI algorithm combined with the currently rec­
ommended method of correcting for multiple comparisons, family wise
error (FWE) corrections and threshold-free cluster enhancement (Alba­
jes-Eizagirre et al., 2019; Smith and Nichols, 2009).
Neuroimaging studies have also examined the neural correlates of
successful emotional episodic memory retrieval, for example, by con­
trasting event-related activity during recognition hits (successful
retrieval) with recognition misses (unsuccessful retrieval) for emotional
stimuli. The neural correlates related to successful retrieval have
received significantly less attention than corresponding processes asso­
ciated with encoding, however, and until recently this has precluded the
application of neuroimaging meta-analysis techniques such as SDM to
summarize findings across studies. Accordingly, retrieval studies have so
far only been reviewed in a qualitative manner (Bowen et al., 2018;
Buchanan, 2007; Dolcos et al., 2017a,b; Kensinger and Ford, 2020).
Because a sufficient number of retrieval studies of successful emotional
episodic memory retrieval now exist to apply the SDM analysis method,
in addition to our meta-analysis of successful encoding, we conducted a
related meta-analysis for emotional episodic memory retrieval. To our
knowledge this is the first such coordinate based meta-analysis of brain
activation related to successful emotional episodic memory retrieval.
In summary, the current meta-analysis had two main goals. The first
goal was to update current understanding of what brain regions are
consistently activated during the successful encoding of emotional
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Neuropsychologia 143 (2020) 107495
episodic memory. In line with past empirical studies and qualitative
reviews (Dolcos et al., 2017a,b; Hamann, 2001; Kensinger and Corkin,
2004; LaBar and Cabeza, 2006), for emotional memory encoding we
expected to find SDM activation associated with the direct
amygdala-mediated route, which has been proposed to include the
amygdala, the hippocampus and its closely interconnected neocortical
regions in the parahippocampal gyrus, and the ventral visual stream
(Eichenbaum et al., 2007; Moscovitch et al., 2016; Squire et al., 2007).
Given the importance of the prefrontal cortex in the prefrontally medi­
ated indirect route, we expected to observe clusters of consistent acti­
vations in this region, as well as in other neocortical regions that have
been associated with this indirect route, such as the parietal cortex
(Dolcos et al., 2017a,b).
Because our inclusion criteria were broadly similar to that used by
Murty et al. (2010) (with a few important differences, discussed below)
and included some overlapping studies, we expected that some of the
major results of this previous study would likely also be found in the
current study. However, we also expected that the inclusion of addi­
tional studies and use of the SDM meta-analysis method would poten­
tially reveal additional, novel regions of consistent activation not
previously reported. Alternately, previously reported regions may not be
robust to these changes and may disappear, particularly those that were
smaller and based on fewer studies.
The second goal was to determine what brain regions are consis­
tently associated with the successful retrieval of emotional episodic
memory. Individual neuroimaging studies and qualitative reviews have
suggested that several brain regions have a greater role in memory
retrieval for emotional episodic memory, including the amygdala, pre­
frontal cortex, and visual processing regions (Bowen et al., 2018;
Buchanan, 2007; Dolcos, 2005; Dolcos et al., 2017a,b; Kensinger, 2004;
Kensinger and Ford, 2020). In addition, in line with the principle of
transfer-appropriate processing, the recapitulation hypothesis stipulates
that memory retrieval engages cognitive processes similar to those that
are present during encoding, and that the extent of reinstatement of
these processes determines the likelihood of retrieval success (Bowen
et al., 2018; Buchanan, 2007; Damasio, 1989; Rugg et al., 2008; Wheeler
et al., 2000). Thus, to the extent that emotional memory encoding
processes are recapitulated during emotional memory retrieval, then
consistent activations in regions involved in emotion processing, mem­
ory formation, attention, perception, and semantic processing during
successful encoding would also be expected to be observed during
retrieval. That is, we expected to observe significant overlap between
the brain correlates of successful encoding and retrieval. On the other
hand, we also expected retrieval-specific activations, since memory
retrieval also engages several unique processes such as memory access,
retrieval monitoring, selection, and subjective aspects such as recollec­
tion, familiarity, and confidence (Buchanan, 2007; Henson, 2005;
Skinner and Fernandes, 2007). To address these two goals, we used the
SDM meta-analysis approach to identify consistent activations across
neuroimaging studies of emotional episodic memory encoding and
retrieval.
2. Methods
Before augmenting the set of neuroimaging papers with papers that
were published after the period included in the previous meta-analysis
(Murty et al., 2010), we first re-evaluated the papers included in that
study to verify that they met our inclusion criteria. Of the 15 papers
identified by Murty et al. (2010), we excluded four as a result of stricter
application of the inclusion and exclusion criteria (see Supplementary
Note for details). In addition to these four papers, one paper that had
been referenced incorrectly in the previous meta-analysis, (Kensinger
and Schacter, 2005b), was included in the current study with the correct
reference (Kensinger and Schacter, 2005a). Additionally, one paper that
was listed by Murty et al. (2010) as only reporting activations in the
medial temporal lobe was included because this study did in fact report
K. Dahlgren et al.
whole brain coordinates (Kensinger and Schacter, 2006a).
Next, to identify additional papers examining the successful encod­
ing of emotional episodic memories, we conducted a literature search
using PubMed in December 2018. The PubMed search for emotional
memory encoding used the following search term: (emotion OR
emotional OR affective OR arousal OR valence) AND (memory OR
recognition) AND (encoding OR encode OR encoded) AND fMRI. This
search of emotional memory encoding papers yielded 526 results.
To identify papers for the meta-analysis of successful episodic
memory retrieval, we used the following search term in PubMed:
(emotion OR emotional OR affective OR arousal OR valence) AND
(memory OR recognition) AND (retrieve OR retrieval OR retrieved) AND
fMRI. This search of emotional memory retrieval papers yielded 419
results. For completeness, we also conducted reverse citation searches
using Google Scholar on review articles that focused on emotional
memory encoding and/or retrieval. These review papers included the
following: Bennion et al. (2013); Bowen et al. (2018); Buchanan (2007);
Dolcos et al. (2017a),b; Hamann (2001). Finally, we also received the
coordinates of the activation maxima from two additional papers
directly from the first authors via email (Bowen and Kensinger, 2017;
Kark and Kensinger, 2019), as the published papers did not report the
contrasts and associated activation maxima coordinates required to
assess the neural correlates of successful emotional episodic memory
encoding and retrieval separately (i.e., these two papers reported reca­
pitulation contrasts that combined both encoding and retrieval).
2.1. Inclusion and exclusion criteria
Papers identified in the database searches were next examined to
determine whether they met criteria for inclusion in our meta-analysis.
Our criteria were specified with respect to the neuroimaging method
used, the sample population included, the types of stimuli presented, the
types of memory tasks used, the contrasts of interest assessed, whether
whole brain coordinates for activation maxima were reported, and
whether behavioral results were reported. Detailed descriptions of these
criteria are described below.
2.1.1. Neuroimaging method
To be included, a study was required to be an event-related fMRI
study using the subsequent memory paradigm (Paller and Wagner,
2002). Positron emission tomography (PET) neuroimaging studies were
excluded because these studies use block designs that do not allow for
the examination of neural activity related to successful encoding or
retrieval for individual trials (Dolcos et al., 2017a,b; Henson, 2005;
Murty et al., 2010). In addition, included studies needed to report the
results of voxel-wise univariate neuroimaging activation analyses.
Functional connectivity and multivariate results (e.g., partial
least-squares analyses) were excluded because their results are qualita­
tively different from univariate activation analyses as they assess con­
nectivity and spatially distributed patterns rather than the voxel-wise
activation data required for SDM analyses.
2.1.2. Sample population
Only studies that reported data from healthy young adult pop­
ulations were included. Studies that compared healthy young adult
populations to other populations were included only if data from the
healthy young adult population was reported separately. Studies that
manipulated factors related to memory strength (i.e., sleep, hormonal,
or pharmacological manipulations) were included if the control condi­
tion or placebo group results were reported separately.
To minimize the potential that within-group effects (non-indepen­
dent sampling from the same group of subjects) could influence the re­
sults of the meta-analyses, we followed current meta-analysis guidelines
regarding the inclusion of multiple contrasts or studies originating from
the same sample (Alegria et al., 2016; Müller et al., 2018; Norman et al.,
2016). When one or more fMRI studies were conducted using the same
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Neuropsychologia 143 (2020) 107495
sample, all appropriate contrasts from all relevant papers were com­
bined into a single contrast. If a study reported more than one emotional
memory-related contrast from the same sample population, contrasts
were combined into a single pooled study/contrast. If a more general
combined contrast was also available, then the more general contrast
was included instead.
2.1.3. Stimuli
Studies were included if they presented emotional stimuli (positive
and/or negative) either alone or paired with another stimulus of either
emotional or neutral valence. Individual stimuli were either words,
objects, faces, scenes, scrambled scenes, or line drawings of scenes.
Alternately, studies were also included if they included neutral stimuli
(objects, words, or scenes) that were paired with (or placed on) a neutral
or emotional background or context (objects, faces, scenes, sentences,
sounds). Because we were interested in the enhancing effect, rather than
the impairing effects of emotion on memory, one study that presented
emotional or neutral objects on neutral backgrounds and only tested
memory for the neutral background was excluded (Bennion et al., 2017),
because memory for neutral backgrounds is typically impaired when
emotional stimuli are presented concurrently at study (Buchanan and
Adolphs, 2002; Reisberg and Heuer, 2004).
2.1.4. Memory tasks
Encoding Tasks: Studies that used incidental or intentional encoding
tasks were included. The encoding tasks for included studies involved
either the presentation of single stimuli, or alternately, the presentation
of two stimuli (either simultaneously or successively). Retrieval tasks:
Studies that used item or associative recognition tasks, recall tasks, or
source memory tasks were included. Excluded tasks: Data from
emotional memory encoding and retrieval tasks were excluded if the
contrasts involved any of the following additional components: auto­
biographical memory, emotion regulation, fear conditioning, reward
and appetitive learning, self-referential processing, or personality trait
associations.
2.1.5. Contrasts of interest
Encoding studies: To be included, studies were required to include
activation contrasts comparing successful episodic encoding of
emotional stimuli to successful encoding of neutral stimuli, or successful
encoding of emotional stimuli to unsuccessful encoding of emotional
stimuli. This included studies with any of the following possible con­
trasts: (emotional subsequent hits – emotional subsequent misses) >
(neutral subsequent hits –neutral subsequent misses) also referred to as
(emotional DM > neutral DM) (DM; difference in memory), emotional
subsequent hits > neutral subsequent hits, or emotional subsequent hits
> emotional subsequent misses (also referred to as emotional DM).
Additionally, we included studies that first contrasted responses to
emotional vs. neutral stimuli and then assessed differences in subse­
quent memory using a parametric regressor (Pais-Vieira et al., 2016) or
studies that first contrasted differences in memory (i.e., the DM effect)
and then assessed the effect of emotion using a parametric regressor
(Cahill, 2004). In cases where results for more than one contrast
assessing emotional DM effects were available, the (emotional DM >
neutral DM) was selected for inclusion.
Retrieval studies: To be included, studies were required to include
activation contrasts comparing successful retrieval of emotional items to
successful retrieval of neutral items, successful retrieval of neutral items
paired with an emotional context to successful retrieval of neutral items
paired with a neutral context, successful retrieval of emotional items to
unsuccessful retrieval of emotional items, or successful retrieval of
neutral items paired with an emotional context to unsuccessful retrieval
of neutral items paired with an emotional context. This included studies
with the following possible contrasts: (emotional hits – emotional mis­
ses) > (neutral hits – neutral misses) also referred to as (emotional DM >
neutral DM), emotional hits > neutral hits, and emotional hits >
K. Dahlgren et al.
emotional misses (also referred to as emotional DM). In cases where
more than one contrast was available, the (emotional DM > neutral DM)
was the preferred contrast.
Valence-specific contrasts: The main goal of this meta-analysis was to
identify brain regions that are consistently activated across studies.
Because there were not enough studies to conduct a sufficiently powered
meta-analysis comparing studies of negative and positive emotional
memory, for our main analysis, we combined results across studies of
positive and negative emotional episodic memory. To minimize non-
independent sampling related to inclusion of multiple contrasts from
the same sample, we followed best practice guidelines (Alegria et al.,
2016; Müller et al., 2018; Norman et al., 2016). If a study reported
encoding or retrieval success-related contrasts separately for both pos­
itive and negative stimuli, then both the positive and negative successful
memory contrasts were included and pooled into a combined memory
contrast. If a study also reported a combined contrast that included both
positive and negative stimuli, this combined contrast was used instead of
any comparable valence-specific contrasts.
Although there were insufficient studies to conduct valence specific
analyses as a primary analysis due to low statistical power, because there
is substantial current interest in determining the valence-specific effects
of emotion on episodic memory, we conducted an exploratory, supple­
mental analysis of studies that directly compared positive encoding
success activity to negative encoding success activity.
Source memory and paired associate recognition contrasts: Papers that
involved a retrieval task requiring a source judgment or paired associate
recognition were included. If a study reported source hit and source miss
contrasts separately, then both contrasts were included and pooled into
a combined memory contrast.
Confidence or recollection/familiarity judgments: Papers that used a
retrieval task requiring a confidence or remember/know judgment
during recognition of a target memory item were included. If a study
reported encoding or retrieval success related contrasts separately for
high and low confidence hits, or for remember and know hits, then both
contrasts were included and pooled into a combined contrast. Any
studies that only reported the results of contrasts between recollection
and familiarity (e.g., [emotional remember – neutral remember] >
[emotional know – neutral know]) were excluded. These contrasts were
excluded because contrasts that subtract out familiarity from recollec­
tion would likely produce a biased and incomplete representation of the
brain regions contributing to encoding and retrieval success effects
because they filter out non-recollection related processes. This criterion
resulted in the exclusion of the data from one study from the encoding
analysis (Ritchey et al., 2019) and the equivalent of one study’s data
from the retrieval analysis. The excluded data from the retrieval analysis
came from two studies that used the same sample population tested at
two different delays, and the data from these two studies would have
been pooled into one data set to avoid non-independence (Sterpenich
et al., 2007, 2009). Thus, effectively, one study for the encoding analysis
and one for the retrieval analysis were excluded.
Canonical hemodynamic response function (HRF): Only contrasts based
on a canonical HRF were included. One included study reported con­
trasts based on a canonical HRF and also provided additional results
from the same study based on a delayed HRF response regressor;
therefore, for this study, only the contrast data corresponding to the
canonical HRF was included (Maratos et al., 2001).
2.1.6. Whole-brain coordinates
Studies that reported activations for the whole brain were included.
Studies that reported regional activations only within the medial tem­
poral lobe, or other specific regions of interest (ROIs), were not included
unless whole brain activation results were available from the author.
Based on recommendations by Müller et al. (2018), when studies re­
ported both whole brain activations and small volume correction (SVC)
analyses for a-priori ROIs, activations from the SVC analyses that did not
also meet the thresholds used for the whole brain analyses were
5
Neuropsychologia 143 (2020) 107495
excluded. Studies that used masking procedures that had the effect of
restricting the whole brain results to less than the whole brain, for
example, by masking the results to include only the ventral affective
network and dorsal executive networks (Dolcos et al., 2013), were
excluded. All included studies reported activation coordinates in stan­
dard stereotactic space (either Montreal Neurological Institute (MNI)
(Evans et al., 1993) or Talairach (Talairach and Tournoux, 1988).
2.1.7. Behavioral testing
Studies were included only if they also reported the results from
behavioral tests assessing episodic memory performance.
2.1.8. Description of included papers
Following application of these selection criteria, the final set of pa­
pers was as follows. For studies of successful encoding of emotional
episodic memory, 25 papers consisting of 32 contrasts (7 pooled con­
trasts), 516 subjects (between 310 and 313 or approximately 60% of
subjects were female but the exact number is unknown as one study did
not provide updated gender distributions after exclusion of participants
from further analyses), and 285 foci were included. A complete list of
these studies and their design characteristics are included in Table 1 (see
Supplemental Table 1 for additional information about the included
encoding studies). For studies of successful retrieval of emotional
episodic memory, 17 papers consisting of 25 contrasts (8 pooled con­
trasts), 310 subjects (between 149 and 152 or approximately 48–49% of
subjects were female but the exact number is unknown as one study did
not provide updated gender distributions after exclusion of participants
from further analyses), and 210 foci were included. A complete list of
these studies and their design characteristics are included in Table 2 (see
Supplemental Table 2 for additional information about the included
retrieval studies).
2.2. Meta-analysis method
2.2.1. Seed-based d mapping
Seed-based d mapping (SDM) SDM-PSI provides a method of con­
ducting statistical inferences on results from multiple studies, with
varying tasks and sample sizes, to find agreement across subject groups
(Albajes-Eizagirre et al., 2019; for information regarding previous ver­
sions of SDM see Radua and Mataix-Cols, 2009; Radua et al., 2012;
Radua et al., 2014). During preprocessing, SDM converts reported
t-values for each peak activation for each contrast into Hedge’s g effect
sizes and their associated variance. Then, for each study, SDM uses
multiple imputation to progressively estimate the upper and lower
bound of probable effect sizes for all voxels using an anisotropic
Gaussian kernel. Voxels close to more than one peak are assigned a
weighted value based on the distance to each peak. Next, SDM uses
multiple imputations of maximum likelihood estimation (MLE) to esti­
mate the most likely effect size and its standard error. To prevent a single
study (or few studies) from driving the results, SDM uses a leave one out
(also known as jackknife) procedure. To address issues of spatial un­
certainty and biases associated with single imputation, each study image
generated during preprocessing undergoes multiple imputations (Rubin,
1987). Then, to allow voxel-wise family wise error rate correction for
multiple comparisons, SDM generates multiple imputations of subject
images and performs subject-based permutation testing. Next, Hedge’s
g-corrected effect sizes are calculated at the group level. Finally, a
random mixed effects model is run with each study weighted by its
variance and between-study heterogeneity.
2.2.2. Meta-analyses
To identify brain regions that were consistently activated during
successful encoding and retrieval of emotional episodic memory, we
used Seed-based d mapping (SDM) SDM-PSI version 6.21 (www.sdmpr
oject.com; Albajes-Eizagirre et al., 2019). For each study, activation
foci, t-statistics, whole-brain thresholds, and sample sizes were entered
K. Dahlgren et al. Neuropsychologia 143 (2020) 107495

Table 1
Studies included in the encoding meta-analysis.
Article N(f) Stimuli Retrieval Task Threshold/ Contrast
Extent

Barnacle et al. (2016) 22 scenes (-/n) free recall p < .005/k ¼ 20 Negative DM > Neutral DM (in mixed emotional and neutral
(22) encoding lists)a
Bisby et al. (2016) 17(?) scenes (-/n) old/new/source p < .001/k ¼ 0 Negative DM > Neutral DM
Bowen and Kensinger 18 words (n)/faces remember/know/ p < .005/k ¼ 10 Emotional Hits > Neutral Hitsa,b
(2017) (12) (þ/ /n)/scenes (þ/ /n) new
Cahill (2004) 15 scenes (-/n) remember/know/ p < .001/k ¼ 4 (HCHs > LCH > Misses) parametrically modulated by arousal
(7) new (reported separately for men and women)
Erk et al. (2003) 10 words (n)/scenes free recall p < .005/k ¼ 0 Negative DM and Positive DM (combined into a single contrast)b
(3) (þ/ /n)
Erk et al. (2005) 10 words (n)/scenes (�) old/new p < .005/cluster Negative DM and Positive DM (combined into a single contrast)b
(3) p < .05
Harvey et al. (2007) 17 scenes (þ/ /n) old/new p < .005/k ¼ 0 Emotional DM > Neutral DM
(8)
Kark and Kensinger 17 line drawings (þ/ /n)/ old/new/ p < .005/k ¼ 17 Negative Hits > Neutral Hits and Positive Hits > Neutral Hits
(2015) (7) scenes (þ/ /n) confidence (combined into a single contrast)
Kark and Kensinger 22 line drawings (þ/ /n)/ old/new/ p < .005/k ¼ 10 Emotional DM > Neutral DMa
(2019) (11) scenes (þ/ /n) vividness
Kensinger and Schacter 16 words (þ/ /n)/objects old/new/source p < .002/k ¼ 6 (Emotional S Hit Emotional S Miss) > (Neutral S Hit Neutral S
(2005a) (9) (þ/ /n) Miss)
Kensinger and Schacter 21 words (þ/ /n)/scenes old/new/source p < .001/k ¼ 5 (Emotional S Hit > Emotional S Miss) and (Emotional S
(2006a) (10) (þ/ /n) Miss > Emotional Miss) combined into a single contrast
Kensinger et al. (2007a) 20 objects (-/n) same/similar/new p < .001/k ¼ 5 Negative DM > Neutral DM
(10)
Kensinger and Schacter 17 objects (þ/ /n) same/similar/new p < .001/k ¼ 5 Emotional DM > Neutral DM
(2008b) (12)
Mickley and Kensinger 20 words (þ/ /n)/scenes old/new/ p < .001/k ¼ 5 Emotional DM > Neutral DM
(2008) (10) (þ/ /n) remember/know
Mickley Steinmetz and 19 scenes (þ/ /n) old/new p < .001/k ¼ 5 Emotional DM > Neutral DM
Kensinger (2009) (11)
Mickley Steinmetz et al. 21 scenes (þ/ /n) old/new p < .001/k ¼ 5 Emotional DM > Neutral DM
(2012) (9)
Pais-Vieira et l. (2016) 17 scenes (þ/ /n) old/new/ p < .005/k ¼ 19 Emotional > Neutral with linear SME regressor
(9) confidence (HCHs > LCHs > Misses)
Parent et al. (2011) 14 scenes (-/n) free recall p < .001/k ¼ 2 Negative DM > Neutral DM (5 min delay and 10 min delay
(0) combined into a single contrast)
Rasch et al. (2009) 57 scenes (þ/ /n) free recall p < .001/k ¼ 3 Negative DM and Positive DM (combined into a single contrast)
(41)
Ritchey et al. (2008) 13 scenes (-/n) old/new/ p < .0025/k ¼ 5 Negative DM > Neutral DM
(7) confidence
Ritchey et al. (2011) 20 scenes (þ/ /n) old/new/ p < .0025/k ¼ 5 Emotional DM > Neutral DM (both deep and shallow encoding)
(10) confidence
Schümann and Sommer 69 scenes (-/n) old/new/ p < .001/k ¼ 10 Negative DM > Neutral DM (short delay and long delay combined
(2018) (69) confidence into a single contrast)
Sergerie et al. (2006) 18 faces (þ/ /n) old/new p < .001/k ¼ 0 Negative DM > Neutral DM (positive stimuli not analyzed)
(9)
Smith et al. (2004) 15 objects (n)/scenes old/new p < .001/k ¼ 5 Emotional Hits > Neutral Hitsb
(8) (þ/ /n)
Talmi et al. (2008) 11 scenes (-/n) old/new/ p < .005/90 mm3 Negative DM > Neutral DM
(5) confidence

Note. Table shows the encoding studies that met inclusion criteria. (N) ¼ total number of subjects, (f) ¼ number of female subjects, (?) indicates that the number of
female participants is unknown because participants were dropped from subsequent analyses without mention of gender of dropped participants, ( ) ¼ negative, (þ)
¼ positive (n) ¼ neutral, DM ¼ Difference in Memory, HCH ¼ high confidence hits, LCH ¼ low confidence hits, R ¼ Remember, K ¼ Know, S¼Source.
a
Indicates that coordinates for this contrast were obtained from the authors and were not reported in the published paper.
b
Indicates that encoded stimuli were neutral items that were paired with an emotional or neutral context.

from contrasts relating to successful emotional memory (encoding or
retrieval). The types of acceptable contrasts that were included are
described in Section 2.1.5, above, and descriptions of the contrasts
included for each study are listed in the corresponding tables for
encoding and retrieval. Prior to statistical analysis, all statistical values
were converted to t-values using SDM’s “convert peaks” utility. If an
included study did not report statistical values for the foci, then the
t-value corresponding to the threshold used to generate the contrast was
entered. Preprocessing was performed according to standard SDM
guidelines, using a 20 mm full width half maximum (FWHM) anisotropic
Gaussian kernel and 2 mm voxel size. After preprocessing, for studies
that reported more than one contrast of interest, the maps that were
generated during preprocessing were combined using SDM’s “combine
image” function. This function creates a map that is the mean of the
effect sizes and variance of the different contrasts (for details, see
supplemental material for Alegria et al., 2016; Norman et al., 2016).
During the main analysis, the number of imputations was set to 50 and
permutations was set to 1000. Voxel-wise results are reported using
threshold-free cluster enhancement family wise error rate (TCFE FWER)
p < .05. The regions listed in the Tables of results for the meta-analyses
were labeled using a combination of the Harvard-Oxford atlas
(http://www.cma.mgh.harvard.edu) and additional neuroanatomical
references for more precise identification of areas such as the medial
temporal lobe subregions (Bouyeure et al., 2018).
2.2.3. Supplemental analyses
In addition to the main meta-analyses, we conducted additional,
supplementary analyses to explore additional questions. To investigate
whether the results of the encoding meta-analysis were similar when
only studies that reported significant emotional memory enhancement

6
K. Dahlgren et al. Neuropsychologia 143 (2020) 107495

Table 2
Studies included in the retrieval meta-analysis.
Article N(f) Stimuli Recognition Task Threshold/Extent Contrast

Bisby et al. (2016) 17(?) scenes (-/n) old/new/source p < .001/k ¼ 0 Negative DM > Neutral DM
Bowen and Kensinger 18 words (n)/faces (þ/ /n)/ remember/ p < .005/k ¼ 10 Emotional Hits > Neutral Hitsa,b
(2017) (12) scenes (þ/ /n) know/new
Erk et al. (2005) 10(3) words (n)/scenes (�) old/new p < .005/cluster Negative DM and Positive DM (combined into a single contrast)b
p < .05
Fenker et al. (2005) 20 words (n)/faces (-/n) remember/ p < .005/k ¼ 0 (Negative R Hits > Neutral R Hits) and (Negative K Hits > Neutral K
(14) know/new Hits) (combined into a single contrast)b
Ford et al. (2014) 27 words (n)/scenes (þ/ /n) old/new p < .005/k ¼ 10 Emotional Hits > Neutral Hitsb
(12)
Kalpouzos et al. (2012) 19(9) scenes (-/n) old/new p < .001/k ¼ 20 Negative DM > Neutral DM
Kark and Kensinger 17(7) line drawings (þ/ /n)/ old/new/ p < .005/k ¼ 10 Negative Hits > Neutral Hits and Positive Hits > Neutral Hits
(2015) scenes (þ/ /n) confidence (combined into a single contrast)
Kark and Kensinger 29 line drawings (þ/ /n)/ old/new/ p < .005/k ¼ 10 Emotional Hits > Neutral Hitsa
(2019) (14) scenes (þ/ /n) vividness
Kensinger and 19 objects (-/n) same/similar/ p < .005/k ¼ 5 Negative DM > Neutral DM {DM defined as (same and
Schacter (2007b) (10) new similar) > miss}
Lewis et al. (2011) 22 objects (n)/scenes (-/n) old/new/source p < .001/k ¼ 10 Negative S Hit > Neutral S Hitb
(12)
Maratos et al. (2001) 12(7) words (n)/sentences old/new p < .001/k ¼ 4 Negative Hits > Neutral Hits and Positive Hits > Neutral Hits
(þ/ /n) (combined into a single contrast)b
Sergerie et al. (2006) 18(9) faces (þ/ /n) old/new p < .001/k ¼ 0 Negative DM > Neutral DM (positive stimuli not analyzed)
Sharot et al. (2004) 13(8) scenes (-/n) remember/ p < .002/k ¼ 19 (Negative R Hits > Neutral R Hits) and (Negative K Hits > Neutral K
know/new Hits) (combined into a single contrast)
Smith et al. (2004) 15(8) objects (n)/scenes (þ/ /n) old/new p < .001/k ¼ 5 Emotional Hits > Neutral Hitsb
Smith et al. (2005) 18(8) objects (n)/scenes (þ/ /n) old/new/source p < .001/k ¼ 5 (Emotional S Hit > Neutral S hit) and (Emotional S Miss > Neutral S
Miss) (combined into a single contrast)b
Smith et al. (2006) 16(8) objects (n)/scenes (-/n) old/new/source p < .001/k ¼ 0 (Negative S Hit > Neutral S Hit) and (Negative S Miss > Neutral S
Miss) (combined into a single contrast)b
Takashima et al. 20(0) scenes (n)/sounds (-/n) old/new/ p < .001/FWE VS Negative Hits > VS Neutral hits (recent and remote combined
(2016) confidence p < .05 into a single contrast)b

Note. Table shows the studies that met inclusion criteria. (N) ¼ total number of subjects, (f) ¼ number of female subjects, (?) indicates that the number of female
participants is unknown because participants were dropped from subsequent analyses without mention of gender of dropped participants, ( ) ¼ negative, (þ) ¼
positive, (n) ¼ neutral, DM ¼ Difference in Memory, R ¼ Remember, K ¼ Know, S¼Source, VS ¼ very sure.
a
Indicates that coordinates for this contrast were obtained from the authors and were not reported in the published paper.
b
Indicates that stimuli presented during the retrieval task were neutral items that were paired with an emotional or neutral context during encoding.

effects were considered, we ran a supplementary analysis excluding
studies that did not show a behavioral enhancement effect for emotional
relative to neutral stimuli (21 out of 25 papers). The specific details for
the excluded papers are listed in Table 1 (Harvey et al., 2007; Kark and
Kensinger, 2015, 2019; Erk et al., 2005).
To identify possible valence-specific effects at encoding, we ran a
supplemental meta-analysis with 6 papers that contrasted successful
positive memory to successful negative memory (as well as the reverse
contrast). This supplemental analysis was exploratory, as 6 studies is
below the recommended guidelines for the minimum number of studies
to have sufficient statistical power (Radua, 2014, 2016, 2018).
Finally, to clarify the interpretation of amygdala activation observed
in the retrieval meta-analysis, we conducted a supplemental meta-
analysis that separately examined SDM activations in the retrieval
meta-analysis according to whether the stimuli presented at retrieval
were emotional items that were also presented at encoding, or neutral
items that were previously paired or associated with a negative item or
context during encoding. Seven studies presented previously encoded
emotional stimuli at test and ten studies presented neutral stimuli at test
that had previously been paired with an emotional item or context (the
latter ten studies are identified in Table 2 by a y following the name of
the contrast).
3. Results
3.1. Behavioral results
All included neuroimaging studies reported the results of behavioral
memory testing that assessed the emotional enhancement effect. Of the
papers that examined successful encoding of emotional episodic mem­
ory, 84% (21/25 papers) showed an emotional enhancement effect.
When these behavioral results for encoding studies were subdivided
based on the valence of the stimuli presented at test, 86% (18/21) of
studies that presented emotional stimuli at test had an emotional
enhancement effect compared to 75% (3/4) of studies that presented
neutral stimuli at test. Of the papers that examined successful retrieval
of emotional episodic memory, 41% (7/17 papers) showed an emotional
enhancement effect. When these behavioral results for retrieval studies
were subdivided based on the valence of the stimuli presented at test,
57% (4/7) of studies that presented emotional stimuli at test had an
emotional enhancement effect compared to 30% (3/10) of studies that
presented neutral stimuli at test.
3.2. Encoding meta-analysis results
SDM meta-analysis revealed four clusters of significant activation
associated with successful emotional episodic memory encoding
(Table 3, Fig. 1, SDM output images are available as Supplementary
Materials and can also be downloaded from https://identifiers.org/ne
urovault.collection:6627). Cluster one included 6916 voxels in the
right medial temporal lobe (amygdala, hippocampus, entorhinal cortex,
perirhinal cortex, and parahippocampal cortex), ventral visual stream
(lateral occipital cortex, inferior temporal gyrus, temporal occipital
fusiform cortex, temporal fusiform cortex, and occipital fusiform gyrus),
basal ganglia (putamen and pallidum) and other regions including the
orbitofrontal cortex, temporal pole, and insula. Cluster two included
4150 voxels in the left medial temporal lobe (amygdala, hippocampus,
entorhinal cortex, perirhinal cortex, and parahippocampal cortex),
ventral visual stream (temporal occipital fusiform cortex and temporal
fusiform cortex), basal ganglia (putamen and pallidum) and other re­
gions including orbitofrontal cortex, temporal pole, and insula. Cluster
three included 542 voxels in the left ventral visual stream (inferior

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K. Dahlgren et al. Neuropsychologia 143 (2020) 107495

Table 3 Table 3 (continued )

Regions showing significant activations during encoding of emotional items, or Cluster Anatomical Regions L/ Voxels Peak
neutral items encoded in emotional contexts. (s) R
x y z Z
Cluster Anatomical Regions L/ Voxels Peak Value
(s) R
x y z Z Temporal Fusiform
Value Cortex
1 Amygdala, R 6916 24 ¡2 ¡14 6.700 40 32 26 2.793
Putamen, Pallidum Cerebellum 12 42 26 2.853
Temporal Pole 36 4 16 5.565 34 54 30 2.701
Orbitofrontal Cortex 22 10 24 5.305 3 Inferior Temporal L 542 ¡54 ¡60 ¡8 3.416
16 4 16 4.303 Gyrus
Perirhinal Cortex 20 4 32 5.278 Lateral Occipital 48 74 12 3.329
26 22 24 2.821 Cortex (inferior)
Inferior Temporal 52 56 18 4.479 Lateral Occipital 44 68 4 2.815
Gyrus Cortex (inferior)
46 42 22 3.265 Lateral Occipital 42 84 0 2.753
42 0 32 2.993 Cortex (inferior)
Entorhinal Cortex 24 6 32 4.160 Lateral Occipital 36 84 12 2.555
Insula 42 12 14 4.091 Cortex (superior)
40 12 2 3.872 Middle Temporal 50 62 6 3.244
Insula, Planum 38 8 14 3.012 Gyrus
Polare 4 Thalamus L 29 8 2 4 3.159
Insula 34 6 6 2.839
Note. Seed-based d mapping threshold free cluster enhancement family-wise
Superior Temporal 44 0 22 4.046
error rate correction threshold p < .05. Table shows all local maxima sepa­
Gyrus, Planum
Polare rated by more than 10 mm. The maximal peak for each cluster is in bold font.
Lateral Occipital 48 64 6 3.925 Coordinates are reported in Montreal Neurological Institute (MNI) with x, y, and
Cortex (inferior) z in the left-right, anterior-posterior, and inferior-superior dimensions,
42 76 16 3.401 respectively.
52 72 12 2.706
44 76 10 2.593
Temporal Occipital 30 46 16 3.756
temporal gyrus, lateral occipital cortex, and middle temporal gyrus).
Fusiform Cortex, Cluster four included 29 voxels in the left thalamus.
Lingual Gyrus
Temporal Occipital 40 48 12 3.457 3.3. Retrieval meta-analysis results
Fusiform Cortex
Middle Temporal 58 54 8 3.575
Gyrus SDM meta-analysis revealed seven clusters of significant activation
44 18 10 2.751 during the successful retrieval of emotional stimuli or neutral stimuli
Hippocampus 18 24 12 3.478 encoded in an emotional context (Table 4, Fig. 2). Cluster one included
32 26 10 3.427
4648 voxels in the left medial temporal lobe (amygdala, hippocampus,
Cerebellum 30 42 32 3.073
Parahippocampal 24 30 18 2.936
entorhinal cortex and perirhinal cortex), prefrontal cortex (inferior
Cortex frontal gyrus, middle frontal gyrus, orbitofrontal cortex, and precentral
Temporal Fusiform 42 28 20 2.722 gyrus), basal ganglia (putamen and pallidum), and other regions
Cortex including the temporal pole, insula, temporal gyrus (inferior, middle,
38 24 30 2.522
and superior) during the successful retrieval of emotional stimuli or
Occipital Fusiform 26 72 24 2.481
Gyrus neutral stimuli encoded in an emotional context. Cluster two included
160 voxels in the right amygdala. Cluster three included 805 voxels in
2 Temporal Pole L 4150 ¡32 8 ¡30 5.127 the left dorsal visual stream (lateral occipital cortex, middle occipital
22 4 30 3.692 cortex, and angular gyrus). It should be noted that two of the local peak
Amygdala 30 0 18 4.775
coordinates in cluster three are labeled as lateral occipital cortex by the
16 0 22 3.430
Orbitofrontal Cortex 26 10 22 4.773 Harvard-Oxford probabilistic atlas but are labeled as angular gyrus in
Insula 40 0 14 4.487 other neuroanatomical references (e.g., the Automated Anatomical La­
Hippocampus 16 14 18 4.300 beling (AAL) atlas, Tzourio-Mazoyer et al., 2002), and in neuroimaging
Hippocampus, 26 34 12 2.760 (Seghier, 2013; Spaniol et al., 2009), neuropsychological (Davidson
Parahippocampal
et al., 2008) and TMS (Bonnici et al., 2018; Yazar et al., 2014, 2017)
Cortex, Lingual
Gyrus studies of episodic memory retrieval. To facilitate comparison with this
Temporal Pole, 40 2 24 4.276 existing literature, we have noted the two cases where lateral occipital
Planum Polare, cortex activation would be alternately identified as left angular gyrus
Middle Temporal
(identified by an * after the angular gyrus label in Table 4). Cluster three
Gyrus
Entorhinal Cortex, 24 10 30 4.005 also contained an additional significant activation identified as the left
Perirhinal Cortex angular gyrus by the Harvard-Oxford atlas. Cluster four included 734
Putamen 28 2 4 3.785 voxels in the right prefrontal cortex (inferior frontal gyrus, precentral
Putamen, Pallidum 18 8 6 3.406 gyrus, and frontal pole). Cluster five included 121 voxels in the right
Parahippocampal 14 36 12 3.529
ventral visual stream (lateral occipital cortex). Cluster six included 22
Cortex
28 26 20 3.239 voxels in the middle temporal gyrus. Cluster seven included 214 voxels
18 26 22 2.925 in the left parietal opercular cortex, planum temporale, central oper­
Temporal Occipital 40 58 20 3.492 cular cortex, and Heschl’s gyrus.
Fusiform Cortex
44 52 28 3.398
44 44 20 3.349

8
K. Dahlgren et al. Neuropsychologia 143 (2020) 107495

Fig. 1. Regions showing significant SDM activations associated with the successful encoding of emotional episodic memory (voxel-wise threshold free cluster
enhancement family wise error corrected, p < .05) are overlaid on a standard single-subject anatomical MRI image from SPM12 (Holmes et al., 1998) (A: axial slices;
B: coronal slices). Intensity color scale indicates Z score values. Coordinates are in MNI space. (For interpretation of the references to color in this figure legend, the
reader is referred to the Web version of this article.)

3.4. Supplemental analysis results
We conducted a supplementary analysis to examine the extent to
which the main encoding analysis results were also observed when only
studies reporting a significant behavioral emotional memory enhance­
ment effect were examined (21 out of 25 encoding studies showed a
behavioral enhancement effect). This analysis revealed broadly similar
activations as the main analysis. Whereas the extent of activations
decreased slightly, nearly all of the original regions remained
significant, with the exception of part of cluster one (specifically, the
right occipital fusiform gyrus and cerebellum). The main findings of the
supplementary analysis were the following: cluster one in the right
medial temporal lobe, and surrounding regions extending to the right
ventral visual stream decreased in size from 6916 voxels to 5142 voxels,
cluster two in the left medial temporal lobe and surrounding regions
increased from 4150 voxels to 4609 voxels. This increase is mostly
attributable to what was previously cluster three in the left ventral visual
stream merging with cluster two; however, the total volume of the

9
K. Dahlgren et al. Neuropsychologia 143 (2020) 107495

Table 4
Regions showing significant activations during retrieval of emotional items, or neutral items encoded in emotional contexts.
Peak

Cluster Anatomical Regions(s) L/R Voxels x y z Z Value

1 Temporal Pole, Orbitofrontal cortex, Insula L 4648 ¡36 4 ¡24 5.287
Temporal Pole, Middle Temporal Gyrus, Superior Temporal Gyrus 48 4 20 5.043
Temporal Pole, Inferior Temporal Gyrus 44 8 34 4.318
Putamen, Pallidum 20 2 6 4.716
Amygdala 26 10 12 3.650
Entorhinal Cortex, Perirhinal Cortex 12 8 28 3.387
Middle Frontal Gyrus, Precentral Gyrus 48 14 30 3.708
Hippocampus 24 8 30 3.549
18 10 22 3.125
14 10 18 3.102
Inferior Frontal Gyrus (pars triangularis) 50 24 18 2.938
Inferior Frontal Gyrus (pars opercularis) 54 10 12 2.922
Inferior Frontal Gyrus (pars opercularis), Central Opercular Cortex 50 18 6 2.796

2 Amygdala R 160 26 2 18 4.864

3 Lateral Occipital Cortex (superior), Middle Occipital Cortex, Angular Gyrusa L 805 ¡42 ¡74 30 4.713
Lateral Occipital Cortex (superior), Angular Gyrusa 44 62 36 4.206
Lateral Occipital Cortex (superior) 48 72 38 4.020
Lateral Occipital Cortex (inferior) 46 72 14 3.219

4 Inferior Frontal Gyrus (pars triangularis) R 734 52 30 4 4.353

Inferior Frontal Gyrus (pars triangularis) 52 26 14 3.492
Inferior Frontal Gyrus (pars opercularis) 54 16 16 3.521
Precentral Gyrus, Rolandic Operculum 48 4 24 3.763
Precentral Gyrus 56 4 34 3.268
Frontal Pole 42 42 2 2.981

5 Lateral Occipital Cortex R 121 54 ¡68 ¡10 4.124

6 Middle Temporal Gyrus R 22 54 ¡56 10 3.944

7 Parietal Operculum Cortex L 214 ¡52 ¡32 18 3.465

Planum Temporale 58 40 20 3.327
Central Opercular Cortex, Heschl’s Gyrus 48 20 14 3.325

Note. Seed-based d mapping threshold free cluster enhancement family-wise error rate correction threshold p < .05. Table shows all local maxima separated by more
than 10 mm. The maximal peak for each cluster is in bold font. Coordinates are reported in Montreal Neurological Institute (MNI) with x, y, and z in the left-right,
anterior-posterior, and inferior-superior dimensions, respectively. Coordinates are labeled using the Harvard-Oxford atlas.
a
indicates coordinates that are labeled as lateral occipital cortex by the Harvard-Oxford atlas but are labeled as angular gyrus by the Automated Anatomical Labeling
(AAL) atlas.

merged clusters is still smaller than the original separate clusters com­ ult.collection:6627). These results should be interpreted with caution
bined. Cluster four in the left thalamus decreased from 29 voxels to 16 because the small number of studies resulted in low statistical power.
voxels. See Supplemental Fig. 1 for a visual representation of these
differences (SDM output images for the analysis of only studies reporting
3.5. Overlap between encoding and retrieval meta-analysis results
a significant behavioral emotional enhancement effect are available as
Supplementary Material and can also be downloaded from https://ide
The SDM maps for successful encoding and retrieval had five clusters
ntifiers.org/neurovault.collection:6627).
of overlapping activation (Table 5, Fig. 3, SDM output images are
We also conducted a supplementary analysis to examine valence
available as Supplementary Materials and can also be downloaded from
specific effects (regions that were more active for positive compared to
https://identifiers.org/neurovault.collection:6627). Cluster one had
negative emotional memory and vice versa) on successful emotional
2272 overlapping voxels in the left medial temporal lobe (amygdala,
episodic memory encoding. This analysis included 6 papers that con­
hippocampus, entorhinal cortex and perirhinal cortex), basal ganglia
trasted successful positive memory to successful negative memory and
(putamen, pallidum), orbitofrontal cortex, insula, and temporal pole.
the reverse contrast. The SDM analysis revealed no valence-specific ef­
Cluster two had 160 overlapping voxels in the right amygdala. Cluster
fects for successful encoding, even at a lenient threshold of p < .001
three had 97 overlapping voxels in the right lateral occipital cortex.
uncorrected. The null results of this supplementary analysis should be
Cluster four had 21 overlapping voxels in the left lateral occipital cortex.
interpreted cautiously, given that the number of studies was substan­
Cluster five had 5 overlapping voxels in the right middle temporal gyrus.
tially below the recommended number of studies for use of SDM.
The Dice similarity score between the SDM maps for successful
The analysis that compared retrieval studies that presented neutral
emotional memory encoding and retrieval was 0.279.
stimuli at test (which had been paired at encoding with an emotional
item or context, 10 studies) to those that presented emotional stimuli
4. Discussion
again during retrieval (7 studies) found that amygdala activation was
observed for the former but not the latter type of study (see Supple­
4.1. Encoding and retrieval SDM results
mental Table 2 for additional brain regions observed for each type of
retrieval task, SDM output images are available as Supplementary Ma­
This study had two primary goals: To update current understanding
terials and can also be downloaded from https://identifiers.org/neurova
of what brain regions are consistently activated during the successful

10
K. Dahlgren et al. Neuropsychologia 143 (2020) 107495

Fig. 2. Regions showing significant SDM activations associated with the successful retrieval of emotional episodic memory (voxel-wise threshold free cluster
enhancement family wise error corrected, p < .05) are overlaid on a standard single-subject anatomical MRI image from SPM12 (Holmes et al., 1998) (A: axial slices;
B: coronal slices). Intensity color scale indicates Z score values. Coordinates are in MNI space. (For interpretation of the references to color in this figure legend, the
reader is referred to the Web version of this article.)

11
K. Dahlgren et al. Neuropsychologia 143 (2020) 107495

Table 5 entorhinal cortex, perirhinal cortex, and parahippocampal cortex

Regions showing overlap between successful encoding and retrieval of
emotional memory.
Cluster Anatomical Regions(s) L/ Voxels
R as well as other temporal regions including the right inferior temporal
1 Amygdala, Hippocampus, Entorhinal Cortex, Perirhinal L 2272
Cortex, Putamen, Pallidum, Insula, Orbitofrontal Cortex,
Temporal Pole, Inferior Temporal Gyrus, Planum Polare
2 Amygdala R 160
3 Lateral Occipital Cortex (inferior) R 97
4 Lateral Occipital Cortex (inferior) L 21
5 Middle Temporal Gyrus R 5
Note. Table lists the brain regions located within areas of overlapping activation
for successful encoding and retrieval of emotional memory. Each cluster in­
dicates a contiguous region of overlap. Number of voxels indicates the number of
voxels within that contiguous cluster.
encoding of emotional episodic memory and for the first time, to our
knowledge, summarize the set of brain regions that are consistently
associated with the successful retrieval of emotional episodic memory.
The meta-analysis found that the successful encoding of emotional
episodic memory was associated with multiple medial temporal lobe
structures known to be critically important for encoding and consoli­
dation of emotional memory including the amygdala, hippocampus,
(Eichenbaum et al., 2007; McGaugh, 2004; Squire, 2004). Outside the
medial temporal lobe, we observed encoding success related activation
in bilateral orbitofrontal cortex, bilateral insula, and bilateral putamen
gyri and bilateral temporal pole. Additional activations were found in
bilateral ventral visual stream (including the lateral occipital cortex,
fusiform cortex, and middle temporal gyri). The meta-analysis of suc­
cessful retrieval of emotional episodic memory found activations in the
medial temporal lobe (bilateral amygdala, left hippocampus, left ento­
rhinal cortex, and left perirhinal cortex), bilateral ventral visual pro­
cessing regions, left dorsal visual processing regions, left angular gyrus,
and prefrontal cortex (bilateral orbitofrontal cortex, bilateral inferior
frontal gyrus, bilateral precentral gyrus, left precentral gyrus, and right
frontal pole). Considerable overlap was observed between the encoding
and retrieval maps in the left medial temporal lobe (amygdala, hippo­
campus, entorhinal cortex and perirhinal cortex), right amygdala, in
ventral visual processing regions (bilateral occipital cortex, right middle
temporal gyrus), left orbitofrontal cortex, insula, putamen, and temporal
pole.
In the following sections, we relate our results to the relevant neu­
roimaging literature on emotional memory, including the previous,
related meta-analysis (Murty et al., 2010), discuss the implications of the

Fig. 3. Regional SDM activations associated with the successful encoding of emotional episodic memory (red regions), the successful retrieval of emotional episodic
memory (green regions), and the overlap between encoding and retrieval SDM activations (blue regions) are overlaid on a standard single-subject anatomical MRI
image from SPM12 (Holmes et al., 1998). (A: axial slices; B: coronal slices). Coordinates are in MNI space. The Dice similarity score between the SDM maps for
successful emotional memory encoding and retrieval was 0.279. (For interpretation of the references to color in this figure legend, the reader is referred to the Web
version of this article.)

12
K. Dahlgren et al.
observed activation clusters associated with successful encoding and
successful retrieval of emotional episodic memory, and connect these
findings to broader theoretical issues related to the neural correlates of
episodic emotional memory.
4.2. Amygdala and medial temporal lobe involvement in emotional
memory encoding
Given the well-established roles of the amygdala and other medial
temporal lobe structures (including the hippocampus, entorhinal cortex,
perirhinal cortex, and parahippocampal cortex) in the amygdala-
mediated route to the enhancement of emotional episodic memory
(Bowen et al., 2018; Cahill and McGaugh, 1998; Hamann, 2009; LaBar
and Cabeza, 2006; McGaugh, 2000, 2004), we expected to find consis­
tent emotional encoding related activations in these regions. Consistent
with these predictions, we observed bilateral SDM activations in the
amygdala, hippocampus, entorhinal cortex, perirhinal cortex and para­
hippocampal cortex. Similar ALE results in the amygdala, hippocampus,
and anterior and posterior parahippocampal gyrus were also reported in
the previous meta-analysis (Murty et al., 2010). The bilateral amygdala
findings further highlight the importance of the amygdala as a key
structure involved in the successful encoding of emotional episodic
memory. Similarly, the increased activity in the hippocampus, entorhi­
nal cortex, perirhinal cortex and parahippocampal cortex associated
with successful emotional episodic memory encoding is consistent with
the findings of previous qualitative reviews and the amygdala-mediated
route for the emotional enhancement of memory, which posits that the
amygdala enhances episodic memory through modulation of
memory-encoding related activity in the hippocampus and its associated
neocortical regions.
When assessing differences between the current results and the
previous meta-analysis (Murty et al., 2010), in addition to the effects
attributable to different datasets (i.e., our larger set of studies), it is
important to consider the fact that because of the major methodological
issues discussed above, the methodology used in this previous study is
no longer recommended for use in meta-analyses. In addition, because
our SDM meta-analysis method used a voxel-wise statistical approach, it
was able to detect small areas of activation, as opposed to the approach
used by Murty et al., which was not able to detect activations smaller
than their arbitrarily chosen minimum cluster size of 100 mm3. Taking
these substantial differences into account, while we identify and discuss
major points of similarity and difference with the previous meta-analysis
(Murty et al., 2010), we primarily focus on the interpretation and im­
plications of the current analyses.
4.3. Other regions associated with successful emotional memory encoding
Considerable evidence indicates that the enhancing effects of
amygdala modulation extend beyond the medial temporal lobe to
modulate both other memory systems, and also sensory systems
including visual cortex (Bowen et al., 2018; LaBar and Cabeza, 2006;
Vuilleumier et al., 2004; Vuilleumier and Driver, 2007). Consistent with
this predicted modulation of sensory cortex, we found SDM activations
in ventral visual stream regions including bilateral lateral occipital
cortex (associated primarily with object perception) and bilateral fusi­
form cortex (associated with face perception) (see Fig. 1, Table 3)
(Grill-Spector et al., 2001; Kanwisher and Yovel, 2006). By comparison,
Murty et al. (2010) also reported ALE clusters in the ventral visual
stream, but the clusters we observed using the SDM method were much
more extensive. As discussed in other reviews, the amygdala has mul­
tiple feedback pathways to multiple parts of the ventral visual stream
(Kark and Kensinger, 2015; LaBar and Cabeza, 2006). The modulation of
visual processing by the amygdala is associated with enhanced percep­
tual processing that ultimately results in enhanced memory for detail
and increased perceived vividness of subsequent episodic memory
retrieval (Kark and Kensinger, 2015; Kensinger et al., 2007a; Kensinger
13
Neuropsychologia 143 (2020) 107495
and Schacter, 2007b). We also observed SDM activations in the bilateral
temporal pole for successful emotional episodic memory encoding. The
temporal pole’s role in emotional memory encoding may reflect its
well-documented role in social and emotional processing as well as se­
mantic memory access (Olson et al., 2007).
Based on previous qualitative reviews and the hypothesized pre­
frontally mediated route to emotional episodic memory enhancement,
we expected to find SDM activation in the prefrontal cortex. However,
although some individual encoding studies contributing to our analysis
did report activation coordinates in the prefrontal cortex, we only
observed significant SDM activation in the bilateral orbitofrontal cortex.
Because the observed orbitofrontal cortex activations were close to
medial temporal lobe activations, we examined whether this activation
originated from the orbitofrontal cortex or alternately, might be an
artifact of spatial smoothing of nearby activations in the medial tem­
poral lobe. Inspection of the locations of peak activations reported in the
individual studies contributing to the meta-analysis indicated that the
activations originated in the orbitofrontal cortex.
In comparison to the current results, Murty et al. (2010) reported two
small ALE clusters in the prefrontal cortex (inferior frontal gyrus and the
anterior middle frontal gyrus). Apart from these bilateral orbitofrontal
cortex activations, we observed fewer SDM clusters in regions than
predicted on the basis of the prefrontally mediated indirect route. One
explanation for why we observed only limited activations corresponding
to the prefrontally mediated, indirect route may be that this route has
been characterized as being less consistently involved in emotional
memory enhancement than the amygdala-mediated route (Bowen et al.,
2018; Dolcos et al., 2017a, 2017b). The role of the prefrontally mediated
route has been reported to depend on both emotional valence and the
level of emotional arousal, with greater prefrontal involvement for
low-arousal, positively valenced stimuli (Bowen et al., 2018; Kensinger
and Corkin, 2004). The majority of the studies analyzed in the current
meta-analysis included either negatively valenced stimuli or a combi­
nation of negative and positive stimuli (see Table 1), and several studies
examined memory for relatively high-arousal stimuli. Both of these
study attributes would tend to reduce the contribution of the indirect
route. Although we attempted to determine if there were
valence-specific effects for emotional episodic memory encoding, our
supplemental analysis revealed no significant findings, likely due to the
small number of relevant studies and consequently low statistical power.
The orbitofrontal cortex has been consistently shown to be involved
in emotion processing, social cognition, and in the emotional enhance­
ment of memory (for reviews see Adolphs, 2001, 2002; Beer et al., 2006;
Dolcos et al., 2017a,b). The orbitofrontal cortex has been proposed to
encode a variety of social and emotional information, ranging from the
subjective value of stimuli, social relevance, and social reward (Dolcos
et al., 2017a,b). Increased orbitofrontal activity, and increased con­
nectivity between the orbitofrontal cortex and the hippocampus, has
been observed for successful encoding and retrieval of names paired
with smiling faces compared to neutral faces (Tsukiura and Cabeza,
2008). Additional evidence for the role of the orbitofrontal cortex in
emotional memory enhancement comes from patients with memory
disorders such as frontotemporal dementia, and Alzheimer’s disease,
which showed correlations between grey matter volume in the right
orbitofrontal cortex and emotional enhancement of memory (Kumfor
et al., 2013). Thus, our findings of significant activations in the orbito­
frontal cortex during encoding likely reflect a variety of emotional and
social processes related to the subsequent enhancement of memory for
emotional stimuli.
We also observed SDM activations in the left and right anterior
insula, the right posterior insula, and part of the left and right putamen.
The insula has been strongly linked with multiple aspects of affective
and social processing, including disgust, empathy, pain, gustation, and
interoceptive awareness of body state (Craig, 2003; Dolan, 2002;
Dupont et al., 2003; Ostrowsky et al., 2002; Shelley and Trimble, 2004;
Singer et al., 2004; Wager and Feldman Barrett, 2004; Wicker et al.,
K. Dahlgren et al.
2003). The recruitment of the insula during successful encoding of
emotional episodic memory thus may reflect the encoding of a range of
affective and social attributes including empathy, emotions, and the
somatic states associated with these emotions.
The putamen, part of the basal ganglia, has multiple functions
including aspects of emotion processing. Patients with Huntington’s
disease, which preferentially impacts the basal ganglia (including the
putamen), often have impaired emotion recognition (Calder et al. 2001;
Sprengelmeyer et al., 1996; Sprengelmeyer, 2007). In addition to
impaired emotion recognition, patients with Huntington’s disease also
have decreased grey matter volume and decreased activation in the
putamen (Dogan et al., 2014). Thus, our findings of increased activity in
the putamen for emotional enhancement of memory are consistent with
the established role of the putamen in emotion processing, which may be
integrated with emotion processing occurring in other regions contrib­
uting to successful encoding.
4.4. Retrieval
Previous qualitative reviews of the neuroimaging literature exam­
ining the retrieval of emotional episodic memory have suggested that
several brain regions are activated during retrieval of emotional stimuli,
including the amygdala, other medial temporal lobe structures including
the hippocampus and the entorhinal, perirhinal, and parahippocampal
cortices, prefrontal cortex, and the ventral visual stream (Buchanan,
2007; Dolcos et al., 2017a,b; Bowen et al., 2018; Kensinger and Ford,
2020). However, to our knowledge, no previous quantitative
meta-analysis has been conducted on this literature to identify signifi­
cant areas of retrieval-related activation for emotional episodic memory.
Here we discuss findings from our meta-analysis of emotional episodic
memory retrieval in relation to the emotional memory retrieval litera­
ture and the broader theoretical context of recapitulation of encoding
processes during retrieval.
4.5. Amygdala and medial temporal lobe involvement in emotional
memory retrieval
Similar to the results of our encoding meta-analysis, which found
activation clusters in both the left and right medial temporal lobe, the
results of the retrieval meta-analysis revealed activation bilaterally in
the amygdala and in memory-related medial temporal lobe regions in
the left hemisphere (hippocampus, entorhinal cortex, and perirhinal
cortex). These findings are in line with those of studies of retrieval of
both laboratory events and studies of autobiographical memory
retrieval, which have consistently implicated the amygdala, hippo­
campus, and other medial temporal lobe regions in successful emotional
episodic memory retrieval (Cabeza and St Jacques, 2007; Dolcos et al.,
2017b; LaBar and Cabeza, 2006). During successful emotional memory
retrieval, increased activity in these regions (Dolcos et al., 2017a,b) as
well as increased functional connectivity specifically between the
amygdala and hippocampus (Smith et al., 2006) have been reported.
These findings suggest that increased regional activation and connec­
tivity in the amygdala and medial temporal lobe play an important role
in successful retrieval of emotional episodic memories, paralleling the
well-established importance of these same regions during successful
emotional memory encoding.
The amygdala activation observed for emotional memory retrieval
may be attributable to multiple potential sources. Because amygdala
activation was prominently observed during encoding, consistent with
the principles of transfer-appropriate processing and recapitulation, the
amygdala activation during retrieval may reflect partial re-activation of
prior encoding processes and affective states. Retrieval activations
reflecting the recapitulation (i.e., “echo”) of both perceptual (Bowen and
Kensinger, 2017; Kark and Kensinger, 2019; Wheeler et al., 2000) and
emotional processing (Todorov et al., 2007) are consistent with the
principle of transfer-appropriate processing, in which successful
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Neuropsychologia 143 (2020) 107495
retrieval involves a recapitulation of a subset of the cognitive and brain
processes active during encoding (Bowen et al., 2018; Rugg et al., 2015;
Staudigl and Hanslmayr, 2019).
Alternately, because some retrieval studies (41%) involved the pre­
sentation of previously encoded emotional stimuli again as recognition
targets, to the extent that more emotionally arousing stimuli are more
likely to be subsequently successfully retrieved, successfully retrieved
items may be more emotionally arousing on average. Given the strong
association between emotional arousal and amygdala activation, these
higher-arousal stimuli would be expected to elicit greater amygdala
activation, an effect that may have contributed to the amygdala acti­
vation we observed. Because only some studies (7/17) presented enco­
ded emotional stimuli again as targets during retrieval (the other studies
presented neutral stimuli at retrieval), we examined the prediction that
studies that presented emotional target items at retrieval would show
amygdala activation whereas those that presented neutral stimuli at
retrieval would not. As the number of studies were lower than the rec­
ommended lower limits of 10 studies, the results are consequently un­
derpowered and should be interpreted cautiously. Contrary to the
prediction that amygdala activation would be observed only for studies
that presented emotional stimuli again as retrieval cues, amygdala
activation was observed for retrieval studies that presented neutral
stimuli as retrieval cues, but not for retrieval studies that presented
emotional stimuli as retrieval cues. Given the preliminary nature of
these findings, further studies will be required to identify the factors that
determine the engagement of the amygdala during episodic emotional
memory retrieval.
4.6. Other regions associated with successful emotional memory retrieval
Similar to the results of our encoding meta-analysis, the retrieval
meta-analysis revealed activation in the ventral visual stream bilaterally
in the lateral occipital cortex and in the right middle temporal gyrus.
These findings are consistent with the idea that the amygdala modulates
processing in sensory regions during both encoding and retrieval
(Bowen et al., 2018; Vuilleumier et al., 2004; Vuilleumier and Driver,
2007). During emotional memory retrieval, the prefrontal cortex may
also exert top-down influences on sensory processing regions (Barcelo
et al., 2000; Vuilleumier and Driver, 2007). Recapitulation of sensory
processing regions that were active at encoding has been suggested to be
more prominent for negative emotional stimuli than for positive stimuli
(Bowen et al., 2018).
We observed SDM activations in the left temporal pole for successful
emotional episodic memory retrieval. These activations may reflect the
retrieval of previously encoded social, emotional, and other semantic
information (Olson et al., 2007). In addition, activation of the anterior
temporal pole has been linked with activation of the retrieval mode
associated with emotional episodic memory (Dolan et al., 2000).
Individual neuroimaging studies and qualitative reviews have also
implicated the prefrontal cortex in modulating medial temporal lobe
activity during emotional memory retrieval, and in mediating processes
such as the retrieval of self-relevant emotional experience (Dolcos et al.,
2017a,b; Kensinger et al., 2007; Ochsner et al., 2005), Consistent with
these qualitative reviews, SDM clusters were observed during retrieval
in bilateral orbitofrontal cortex and the bilateral dorsolateral prefrontal
cortex. Activation of orbitofrontal cortex associated with successful
emotional memory retrieval may reflect the recapitulation of the social
and emotional processing that occurred originally during encoding
(Dolcos et al., 2017a,b). The dorsolateral prefrontal cortex is strongly
implicated in a variety of episodic memory retrieval processes such as
selection and monitoring (Moscovitch et al., 2016; Wheeler et al., 1997).
The role of the prefrontal cortex in successful encoding and retrieval of
emotional episodic memories has also been suggested to depend on
factors such as emotional valence (Bowen et al., 2018; Dolcos, Katsumi,
Weymar, et al., 2017; Kensinger and Corkin, 2004; Maratos et al., 2001).
Activation of the insula during successful emotional memory
K. Dahlgren et al.
retrieval may reflect recapitulation of the emotional, somatic, and
cognitive processing that previously occurred during encoding
(Buchanan, 2007; Engen and Singer, 2013; Menon and Uddin, 2010;
Kurth et al., 2010; Uddin et al., 2017). In addition to emotional and
somatic processing, the insula has also been linked to aspects of episodic
memory retrieval (Kurth et al., 2010; Spaniol et al., 2009, Kim, 2013).
Lateral parietal cortex (including the angular gyrus) has been shown
to have a consistent role in neuroimaging studies of episodic memory
retrieval (Vilberg and Rugg, 2008; Wagner et al., 2005). Though some
aspects of its role in memory retrieval remain unclear, there is
compelling evidence that the left angular gyrus supports subjective as­
pects of episodic memory retrieval such as confidence, subjective
re-experiencing of a memory, and the recollection component of
recognition memory. Neuropsychological studies have reported that
lateral parietal lesions are associated with a selective reduction in the
recollection component of recognition memory (Davidson et al., 2008),
and reduced ability to retrieve episodic details during free recall (Ber­
ryhill et al., 2007). TMS studies that have disrupted left angular gyrus
function have reported a selective reduction in the number of internal
memory details retrieved during free recall of autobiographical mem­
ories (Thakral et al., 2017) and also a reduction in the number of
memories retrieved from a first person perspective (compared to a third
person perspective) (Bonnici et al., 2018). TMS to the left angular gyrus
has also been shown to reduce memory confidence (i.e., a subjective
aspect of memory) but not memory accuracy (Yazar et al., 2014). These
findings suggest that the left angular gyrus supports subjective aspects of
episodic memory retrieval. Because the retrieval of emotional episodic
memories would be expected to involve greater subjective
re-experiencing of subjective emotional content, this is consistent with
our observation of an SDM activation cluster for retrieval that included
the left angular gyrus during emotional episodic memory retrieval.
4.7. Behavioral emotional memory effects
Consistent with the typical enhancing effect of emotion on memory,
the majority (84%) of studies included in the meta-analysis of successful
emotional episodic memory encoding reported significantly better
subsequent memory for emotional items than neutral items. On the
other hand, fewer retrieval studies reported a significant emotional
enhancement of memory (41%). One reason for this lower frequency of
emotional memory enhancement in the retrieval studies may be related
to the relationship between encoding and retrieval conditions in each
type of study. Substantially more encoding studies presented emotional
stimuli at both encoding and retrieval (84%) compared to 41% of
retrieval studies. In cases where emotional stimuli were not re-presented
at retrieval, neutral stimuli were presented during retrieval, thus testing
for the indirect effects of emotion on memory for neutral stimuli. As
noted above in section 3.1, behavioral enhancement effects were more
prominent for those encoding and retrieval studies where emotional
stimuli were presented again at test (relative to cases where neutral
stimuli were presented at test.)
4.8. Overlap between successful emotional memory encoding and retrieval
The SDM activations for encoding and retrieval overlapped in the left
medial temporal lobe (amygdala, hippocampus, entorhinal and peri­
rhinal cortices), right amygdala, left orbitofrontal cortex, left insula, left
basal ganglia, left temporal pole, and bilateral ventral visual stream
(bilateral lateral occipital cortex and right middle temporal gyrus). This
overlap in the medial temporal lobe highlights the key importance of the
amygdala and hippocampus in both encoding and retrieval of emotional
episodic memory. Additionally, the overlapping bilateral activation in
the ventral visual stream is consistent with proposals that the amygdala
plays a role in the emotional modulation of activity in visual processing
regions not only during encoding but also during retrieval of emotional
episodic memory (Bowen et al., 2018; Vuilleumier et al., 2004;
15
Neuropsychologia 143 (2020) 107495
Vuilleumier and Driver, 2007). The observed overlap in the orbito­
frontal cortex and temporal pole, regions that are strongly implicated in
emotional and social processing, is consistent with previous literature
implicating both regions in emotional episodic memory (Adolphs, 2001,
2002; Beer et al., 2006; Olson et al., 2007). Finally, these overlap results
are broadly consistent with the principle that successful retrieval in­
volves the recapitulation of a subset of processes present during
encoding (Bowen et al., 2018; Rugg et al., 2015; Staudigl and Hansl­
mayr, 2019).
5. Limitations and future directions
A number of limitations of this study stem from limitations of the
CBMA meta-analytic methods. The encoding and retrieval meta-
analyses should be interpreted as providing a summary of memory-
related activations that are robust across studies and experimental var­
iables, rather than as identifying all regions that are involved in these
memory processes. This is because the SDM method can only identify
activations that are relatively invariant across studies despite variations
in stimulus, task, and other variables. Although the SDM method can be
used to assess the role of different variables on activation, there are
frequently not enough relevant studies to assess the role of such vari­
ables, as was the case in the current study. In this respect, qualitative
reviews can complement the findings of current study by identifying
regions whose role in successful emotional encoding and retrieval is
more variable across studies.
Although several studies have reported key differences between the
brain correlates of emotional episodic memory for negative vs. positive
emotional stimuli (Dolcos et al., 2004; Kensinger and Schacter, 2006b;
LaBar and Cabeza, 2006; Mickley and Kensinger, 2008), there were not
enough relevant papers available to conduct sufficiently powered
meta-analyses comparing memory for negative and positive emotional
stimuli. Our exploratory analysis of this issue for encoding success
yielded null results. More definitive conclusions regarding
valence-specific effects will be possible in the future as more relevant
studies are reported. Similarly, although there has been considerable
interest in potential sex differences in the brain regions involved in
successful emotional episodic memory encoding, there were not enough
studies that reported separate results for men and women to address this
issue in the current study (Cahill, 2004, 2006; 2012; Canli et al., 2002).
Our encoding meta-analysis averaged results across studies that varied
considerably in the proportions of male and female subjects and found
robust bilateral amygdala SDM clusters. This finding suggests that,
despite several prior findings of sex differences in the lateralization of
amygdala activity associated with successful encoding of emotional
episodic memory (i.e., the left but not the right amygdala associated
with successful encoding for emotional memory in women and the
opposite pattern in men (Cahill, 2004; Canli et al., 2002), activation in
both the left and right amygdalae is consistently associated with
encoding success for emotional episodic memory even when results are
combined across females and males.
A question for further investigation is whether successful encoding or
retrieval of emotional episodic memory may be associated with
decreased activation in some regions involved more generally in episodic
memory processing. Given the findings from other cognitive domains
that show reciprocal inhibition of brain processes associated with
emotion and cognition, it would be prudent to explore the possibility
that successful emotional episodic memory encoding and retrieval may
be associated with decreased activation in some brain regions (Bush
et al., 2000; Jack et al., 2013; Northoff et al., 2004). Because few studies
report the results of reverse activation contrasts (e.g., neutral greater
than emotional memory), it was not possible to address this issue in the
current study. Future neuroimaging studies comparing emotional
episodic memory encoding and retrieval success should also report these
reverse contrasts, to allow for further investigation of this question.
Our inclusion criteria excluded studies of autobiographical memory
K. Dahlgren et al.
retrieval, due to the large differences in the paradigms used between
studies that examined retrieval of laboratory-presented events and those
that examined autobiographical memory retrieval. For example, the
retrieval analysis focused on successful vs. unsuccessful episodic mem­
ory retrieval, a contrast that has been a focus of laboratory-based
memory studies, but which is typically not assessed in autobiograph­
ical memory studies. Because a previous meta-analysis concluded that
there are substantial differences in the neural correlates of episodic
memory for stimuli presented in laboratory paradigms vs. those asso­
ciated with autobiographical memory (McDermott et al., 2009), and in
line with the exclusion criteria used in the previous related
meta-analysis (Murty et al., 2010) we excluded studies of autobio­
graphical memory. Given the focus on basic memory mechanisms in
healthy young adults, the current study also excluded data from clinical
populations and older adults. A promising direction for future research
would be to examine how the regional SDM activations reported here in
healthy adults are altered or biased with cognitive aging and in clinical
disorders such as PTSD and depression.
6. Conclusion
The results of the two meta-analyses in the current study reinforce
and corroborate the importance of the amygdala and medial temporal
lobe structures in both the encoding and retrieval of emotional episodic
memory. The findings also point to the consistent involvement of re­
gions outside the medial temporal lobe in successful encoding and
retrieval, including regions involved in visual perception (ventral visual
stream), interoception (insula), and emotion (insula, orbitofrontal cor­
tex, and putamen). Many of these same regions that were active during
encoding were also active during retrieval (medial temporal lobe, insula,
orbitofrontal cortex, putamen, ventral visual stream). In addition to
these regions that were active for both encoding and retrieval of
emotional memory, regions involved in episodic memory retrieval
(angular gyrus), and emotional memory retrieval (dorsolateral pre­
frontal cortex), were also consistently involved in emotional episodic
memory retrieval. These findings support the idea that although some of
the processes present at encoding are recapitulated to some extent, that
emotional memory retrieval also involves retrieval specific processes
that are not shared with encoding. Future research should address the
role of several factors such as emotional valence in modulating the
neural correlates of emotional memory, particularly for emotional
memory retrieval, which has received relatively less attention to date
than encoding.
CRediT authorship contribution statement
Kristina Dahlgren: Conceptualization, Methodology, Formal anal­
ysis, Writing - original draft, Visualization. Charles Ferris: Conceptu­
alization, Methodology, Formal analysis, Writing - original draft.
Stephan Hamann: Conceptualization, Methodology, Formal analysis,
Writing - original draft, Supervision.
Acknowledgements
We would like to thank Vishnu Murty for information regarding the
Murty et al. (2010) meta-analysis. We would also like to thank Sarah
Kark, Holly Bowen, and Deborah Talmi for providing unpublished co­
ordinate data. We would like to thank research assistants Erin Morrow,
Sarah Taha, Jessie Kwong, and Alice Yang for assistance with selecting
and acquiring neuroimaging coordinate data.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.neuropsychologia.2020.107495.
16
Neuropsychologia 143 (2020) 107495
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