The Neural Correlates of Trauma Related Autobiographical Memory in Posttraumatic Stress Disorder: A Meta Analysis

Received: 23 July 2019 | Revised: 2 October 2019 | Accepted: 6 November 2019
DOI: 10.1002/da.22977
REVIEW
The neural correlates of trauma‐related autobiographical

memory in posttraumatic stress disorder: A meta‐analysis
Janine Thome1,2 | Braeden A. Terpou3 | Margaret C. McKinnon4,5,6 | Ruth A. Lanius1,3
1
Department of Psychiatry, Western
University, London, Ontario, Canada Abstract
2
Department of Theoretical Neuroscience, Background: Autobiographical memory (AM) refers to memories of events that are
Central Institute of Mental Health Mannheim,
personally relevant and are remembered from one’s own past. The AM network is a
Medical Faculty Mannheim, Heidelberg
University, Heidelberg, Germany distributed brain network comprised largely by prefrontal medial and posteromedial
3
Department of Neuroscience, Western cortical brain regions, which together facilitate AM. Autobiographical memories with
University, London, Ontario, Canada
4
high arousal and negatively valenced emotional states are thought to be retrieved
Mood Disorders Program, St. Joseph’s
Healthcare, Hamilton, Ontario, Canada more readily and re‐experienced more vividly. This is critical in the case of trauma‐
5
Department of Psychiatry and Behavioural related AMs, which are related to altered phenomenological experiences as well as
Neurosciences, McMaster University,
Hamilton, Ontario, Canada
aberrations to the underlying neural systems in posttraumatic stress disorder (PTSD).
6
Homewood Research Institute, Guelph, Critically, these alterations to the AM network have not been explored recently and
Ontario, Canada have never been analyzed with consideration to the different processes of AM, them
Correspondence being retrieval and re‐experiencing.
Ruth A. Lanius, Department of Psychiatry, Methods: We conducted a series of effect‐size signed differential mapping meta‐
Western University, University Hospital
(Room C3‐103), 339 Windermere Rd., London, analyses across twenty‐eight studies investigating the neural correlates of trauma‐
ON., Canada N6A 5A5. related AMs in participants with PTSD as compared with controls. Studies included
Email: [email protected]
either trauma‐related scripts or trauma‐related materials (i.e., sounds, images,
Funding information pictures) implemented to evoke the recollection of a trauma‐related memory.
Canadian Institutes of Health Research,
Grant/Award Numbers: 137150, 97914; Results: The meta‐analyses revealed that control and PTSD participants displayed
Mitacs; CIMVHR greater common brain activation of prefrontal medial and posteromedial cortices,
respectively. Whereby the prefrontal medial cortices are suggested to facilitate
retrieval monitoring, the posteromedial cortices are thought to enable the visual
imagery processes of AM.
Conclusions: Taken together, reduced common activation of prefrontal cortices may
be interpreted as a bias toward greater re‐experiencing, where the more salient
elements of the traumatic memory are relived as opposed to retrieved in a controlled
manner in PTSD.
KEYWORDS
autobiographical memory, autobiographical memory network, functional magnetic resonance
imaging, meta‐analysis, posttraumatic stress disorder, trauma
1 | INTRODUCTION
Memory is the process by which information is extracted through

experience to facilitate and to inform future action (Markowitsch &
Janine Thome and Braeden A. Terpou contributed equally to this study.
Depress Anxiety. 2019;1–25. wileyonlinelibrary.com/journal/da © 2019 Wiley Periodicals, Inc. | 1

2 | THOME ET AL.
Staniloiu, 2011). The information is encoded within multiple memory project the perceived self into past experiences to examine and to
systems and is retrieved when the information holds value to the hypothesize our own actions, intentions, and emotions at the time of
present moment (Corkin, 1968; Ferbinteanu, 2018; Penfield & recollection (Markowitsch & Staniloiu, 2011; Wheeler, Stuss, &
Milner, 1958; Scoville & Milner, 1957; Squire, 2004). The memory Tulving, 1997).
literature differentiates between two classes of memory on the basis To engage autonoetic consciousness, AM relies on a distributed
of their conscious awareness during retrieval. Whereby explicit brain network, which includes the hippocampus and parahippocam-
memory is consciously retrieved, implicit memory does not require pal cortices, medial and lateral prefrontal cortices, posterior parietal
conscious awareness during retrieval (Schacter & Tulving, 1994; and posteromedial cortices, and visual processing regions (Buckner &
Squire & Dede, 2015; Tulving, 1987, 2007). Explicit memories Carroll, 2007; Cabeza & St Jacques, 2007; Svoboda, McKinnon, &
represent personal events that are associated with specific spatial Levine, 2006). Notably, the AM network is hypothesized to be
and temporal characteristics (i.e., episodic memory) as well as our predominantly left‐lateralized (Svoboda et al., 2006), and overlaps
general knowledge of facts, concepts, and ideas that are learned over partially with the default‐mode network (DMN). The DMN is an
the lifetime (i.e., semantic memory). By contrast, implicit memories intrinsic connectivity network composed of midline prefrontal and
represent learned reactions to the external world (i.e., learned posterior parietal cortices, recruited during AM, self‐referential
contingency of events, procedural patterns, priming) and do not have processing, and internal cognition (Menon, 2011). The DMN, and
generally an available mental representation that can be verbalized related AM network, are comprised largely by two cortical
consciously (Kandel, Dudai, & Mayford, 2014; Kandel, Schwartz, subsystems that contribute to the expression of an AM. Whereas
Jessell, Siegelbaum, & Hudspeth, 2012; Squire & Dede, 2015; Tulving, the dorsal‐medial subsystem (i.e., anterior, lateral temporal, orbito-
1987). Implicit memory systems are engaged rapidly and are thought frontal, prefrontal cortices) is thought to underlie the processing and
to rely on more evolutionarily conserved neural structures to elicit the maintenance of abstract representations of cognitive and of
their learning and memory effects (Squire, 2004), whereas explicit schematic information, the medial‐temporal subsystem (i.e., para-
memory systems are expressed more in large‐scale, phylogenetically hippocampal gyrus, restrosplenial, and posterior parietal cortices)
recent cortical networks (Kim, 2012; Rovee‐Collier, Hayne, & contributes more to perceptual and visual imagery features of
Colombo, 2001; Spreng & Grady, 2010). The harmonious interaction self‐related information as expressed in AMs (Cabeza & St Jacques,
of explicit and of implicit memory systems is thought to facilitate the 2007; St Jacques, Kragel, & Rubin, 2011; Svoboda et al., 2006).
development of our emotional, cognitive, and self‐related processing These dissociable cortical subsystems are also thought to
systems, which critically seem to be affected by traumatic events contribute disproportionately to retrieval and re‐experiencing
(Brewin, 2011, 2014; Ehlers & Clark, 2000; Schacter & Tulving, 1994; processes during AM (Araujo, Kaplan, & Damasio, 2013; Buckner &
Squire, 1987; Squire & Dede, 2015; Tulving, 2002; Van der Kolk & Carroll, 2007; Cabeza & St Jacques, 2007; Svoboda et al., 2006).
Fisler, 1995). Here, the AM literature distinguishes between retrieval phases
(i.e., the active and the controlled process of constructing an AM) and
re‐experiencing phases of AM (i.e., the elaboration of the perceptual,
1.1 | Autobiographical memory (AM)
sensory, and emotional elements of a memory by which reliving
AM is a form of explicit memory involving events that are personally sensations are experienced; Addis, Wong, & Schacter, 2007; Botzung,
relevant and are remembered from one’s own past (Brewer, 1986; Denkova, Ciuciu, Scheiber, & Manning, 2008; Cabeza & St Jacques,
Squire & Dede, 2015). AM incorporates both episodic and semantic 2007; St Jacques, Botzung, Miles, & Rubin, 2011). The former and the
components of explicit memory. Specifically, episodic components of latter phase are hypothesized to be expressed predominantly within
AM involve recollections of experiences specific in time and in place, the dorsal‐medial and the medial‐temporal subsystem, respectively
with accompanying mental and emotional features, including a (Buckner & Carroll, 2007; Cabeza & St Jacques, 2007; Svoboda et al.,
subjective sense of personal continuity across time (Levine, Svoboda, 2006). Re‐experiencing follows generally the retrieval of an AM;
Hay, Winocur, & Moscovitch, 2002; Tulving, 1987). By contrast, however, memories of very high arousal can often engage re‐
semantic components involve information about the world and experiencing processes rapidly—seemingly without the controlled
oneself that are independent of time and of place, such as self‐ retrieval (Ehlers, Hackmann, & Michael, 2004). Although the
relevant facts, traits, and general knowledge (Willoughby, Desrocher, distinction between these phases is important, there are often
Levine, & Rovet, 2012). The integration of these explicit memory inconsistencies during data generation and reporting of the neural
components is thought to allow for AMs to be expressed in narrative correlates associated with AM, which make it difficult to tease apart
form, where self‐relevant information and events associate to these processes (Botzung et al., 2008; Piolino, Desgranges, &
produce a sense of self (Conway & Pleydell‐Pearce, 2000; Levine Eustache, 2009). Oftentimes, the delineation between experimental
et al., 2002). This emergent sense of self is synonymous with, or phases is made by way of an arbitrary cut‐off time that denotes when
related to, the function of autonoetic consciousness (Piolino et al., a participant should have retrieved the memory and is now re‐
2006; Prebble, Addis, & Tippett, 2013; Tulving, 1985)—emerging only experiencing its more salient elements, whereas other studies are
when a child has developed a sense of self (Fivush, 2011; Reese, self‐paced (i.e., ask participants to press a button to signify they are
2002). Here, autonoetic consciousness refers to the human ability to now re‐experiencing the AM). The improved standardization of these
THOME ET AL. | 3
AM paradigms can facilitate a stronger understanding of the 1.2 | Posttraumatic stress disorder (PTSD) and the
processes related to AMs in healthy and in disordered populations AM network
(Addis et al., 2007; Botzung et al., 2008; Piolino et al., 2009; St
PTSD is a disorder characterized by hypervigilance, hyperarousal,
Jacques et al., 2011).
and, in some cases, dissociative symptoms following a traumatic
The ease of retrieval of an AM is thought to be mediated by the
experience (APA, 2013). A hallmark feature of the disorder is the
(emotional) significance of the memory (Talarico, LaBar, & Rubin,
intrusive re‐experiencing of the trauma memory, often following
2004; Williams et al., 2007), with arousal, valence, and consequenti-
exposure to trauma‐related stimuli (APA, 2013). Re‐experiencing
ality serving as three factors that contribute to its (emotional)
symptoms are thought to be evoked through the reestablishment of
significance (Finkenauer et al., 1998). Whereas arousal is thought to
the physiological, psychological, and emotional state of the individual
reflect the degree of physiological response generated during
that occurred during the original encoding (Brewin, 2018).
retrieval, valence considers the positivity or the negativity of the
Experimentally, AMs of trauma are studied through the exposure
event (Conway, 2013; Conway et al., 1994; Kensinger & Corkin,
of often personalized and trauma‐related stimuli to participants with
2004). The arousal and valence dimensions are often considered
PTSD (Bremner, Narayan, et al., 1999; Britton, Phan, Taylor, Fig, &
perpendicular, where different combinations of these two factors
Liberzon, 2005; Dahlgren et al., 2018; Lanius et al., 2002; Liberzon
associate to produce an array of different emotions (Bliss‐Moreau,
et al., 1999; Rauch et al., 1996; Shin et al., 1997). The stimuli used
Williams, & Santistevan, 2019; Lang, Greenwald, Bradley, & Hamm,
vary, but are generally in the form of trauma‐related images (Cwik,
1993; Russell & Mehrabian, 1977; see also Kensinger & Corkin, 2004;
Sartory, Nuyken, Schurholt, & Seitz, 2017; Morey et al., 2009; Zhang
Russell, 1980). These factors are thought to contribute to memory
et al., 2011), trauma‐related sounds (Liberzon et al., 1999; Pissiota
enhancement via dissociable neural systems, with arousal and
et al., 2002), or script‐driven imagery, which involves presenting a
valence dependent primarily on amygdalar‐hippocampal systems
short, verbal description of an individual’s trauma story to facilitate
and amygdalar‐prefrontal systems, respectively (Dolcos, LaBar, &
the retrieval of the fuller memory (Hopper, Frewen, van der Kolk, &
Cabeza, 2004; Kensinger & Corkin, 2004). On the other hand,
Lanius, 2007; Ke et al., 2015; Lanius et al., 2002; Rauch et al., 1996).
consequentiality is a factor concerned with the self‐relevance and the
During the presentation of these stimuli, it is crucial to consider
personal significance of the memory (Conway et al., 1994; McGaugh,
whether brain function is measured during or following the exposure
2004), where AMs with greater personal significance are retrieved
to trauma‐related stimuli. Whereas the former is thought to relate
more quickly and with greater detail (Brown & Kulik, 1977; Kelley
more to retrieval processes, the latter is associated more strongly
et al., 2002; Pezdek, 2003; Rogers, 1977). Generally, AMs with very
with the re‐experiencing processes of AM (see, e.g., St Jacques et al.,
high arousal and either a strong negative or a positive valence are
2011). Notably, trauma‐related AMs are thought to display greater
associated with increased reports of vividness during retrieval as well
altered retrieval and re‐experiencing processes as compared with
(Kelley et al., 2002; Pezdek, 2003; Quevedo et al., 2003). Historically,
nontraumatic, neutral memory recollection, which is reflected in the
highly arousing AMs of this nature are often referred to as “flashbulb
abnormal recruitment of the underlying memory systems in PTSD
memories,” on account of their vivid and, in some cases, intrusive
(McKinnon et al., 2015). These differences are to be discussed, both
retrieval (Brown & Kulik, 1977; Conway, 2013; Conway et al., 1994).
phenomenologically and in terms of the underlying neural systems, to
Despite increased reports of vividness, highly arousing and valenced
follow.
memories do not aid indiscriminately in the retrieval of an AM
With respect to altered AM characteristics, PTSD is often related
(Finn & Roediger, 2011; Sharot & Phelps, 2004). For instance,
to greater re‐experiencing of trauma‐related AMs as compared with
amygdala activation, a reliable indicator of the highly arousing and
trauma‐exposed or healthy control subjects (Brewin, 2015, 2018;
the negatively valenced fear state, is shown to boost the retrieval of
Ehlers & Clark, 2000; Ehlers et al., 2004; van der Kolk & Fisler, 1995).
certain memory characteristics. In particular, increased amygdala
As mentioned, re‐experiencing is identified by strong sensory and
activity is associated with enhanced reality‐monitoring accuracy as
emotional features, which appear to lack the perspective and the
well as reduced memory distortion of emotional as compared with
surrounding context of the trauma memory (Ehlers & Clark, 2000).
neutral stimuli (Kensinger & Schacter, 2005, 2006). Although
Here, Elbert and Schauer (2002) make a distinction between the hot
amygdala activity is thought to enhance the retrieval of emotional
(i.e., sensory, emotional) and the cold (i.e., cognitive, contextual)
stimuli, this enhancement couples strongly with a reduction in the
features of an AM and suggest that trauma memories are the result
retrieval of stimuli presented before the emotional cue (Holland &
of a disconnect, or a fragmentation of these components (Berntsen,
Kensinger, 2010; Strange, Hurlemann, & Dolan, 2003). This observa-
Willert, & Rubin, 2003; Brewin, 2015). In turn, some trauma‐related
tion is in keeping with the claim that negatively valenced arousal
AMs in PTSD are thought to remain in a state‐dependent,
increases the attentional processing of emotional, item‐specific
emotionally charged form that exhibits strong priming to trauma‐
stimuli, while also decreasing the processing of neutral, contextual‐
related cues (Arntz, de Groot, & Kindt, 2005; Grey & Holmes, 2008;
based stimuli presented concurrently (Phelps, Ling, & Carrasco, 2006;
Kleim, Ehring, & Ehlers, 2012; Michael, Ehlers, & Halligan, 2005).
Storbeck & Clore, 2008). The association between arousal, valence,
Increasing evidence assessing the characteristics of these AMs have
and memory is of critical interest, particularly in the case of a trauma‐
revealed that participants with PTSD report more vivid recollections
related memory.
4 | THOME ET AL.
of their traumatic memory in terms of more intense sensory and reports of functional activation gathered during the retrieval and
emotional modalities as compared with trauma‐exposed and healthy the re‐experiencing phases of trauma‐related AM in participants
control subjects (Berntsen et al., 2003; Crespo & Fernandez‐Lansac, with PTSD.
2016; O’Kearney & Perrott, 2006). Moreover, the likelihood to
engage in strong re‐experiencing during trauma‐related AM is found
2 | M A T E R I A L S AN D M E T H O D S
to correlate positively with PTSD symptom severity (Berntsen et al.,
2003). Interestingly, participants with the highest PTSD symptom
2.1 | Study selection
severity also report that their trauma memory had become a part of
their identity (Berntsen & Rubin, 2007; Berntsen et al., 2003). These The present meta‐analysis examines the neural correlates of trauma‐
results have since been replicated in a sample of veterans with PTSD related AM, where studies are considered that investigate the
as well as a sample of adult survivors of childhood sexual abuse who retrieval as well as the re‐experiencing of trauma‐related AMs in
would go on to develop PTSD (Brown, Antonius, Kramer, Root, & participants with PTSD as well as in control subjects. Of note, we
Hirst, 2010; Robinaugh & McNally, 2011). Taken together, these conducted separate meta‐analyses, including a meta‐analysis across
findings support the claim of the centrality of trauma to personal all identified studies investigating trauma‐related AM, as well as
identity in participants with PTSD, which is likely to be mediated by analyses that investigate neural activation during the retrieval as well
the AM network. as the re‐experiencing of trauma‐related AMs, independently.
These altered phenomenological characteristics of trauma‐ However, this distinction has to be interpreted with caution, since
related AMs are reflected, in part, by the underlying neural the categorization is based mainly on the experimental time course
systems recruited during retrieval in PTSD. To this point, (i.e., neural response during as compared with after exposure of the
Sartory et al. (2013) conducted a meta‐analysis where they trauma‐related AM material, which has been related to the retrieval
compiled reports of brain activation within trauma‐related phase (i.e., construction) and the re‐experiencing phase (i.e., elabora-
symptom provocation paradigms across nineteen studies that tion), respectively), without a qualitative assessment of the indivi-
included participants with PTSD as well as trauma‐exposed dual’s subjective experience per se.
controls. For studies included in the meta‐analysis, however, Primary research articles were identified until January of 2019
Sartory et al. did not differentiate between those that scanned (first publication appeared in 1996). Search databases included
during (i.e., retrieval) or following (i.e., re‐experiencing) trauma‐ PubMed, Web of Science, PsycINFO, and Medline. A combination of
related stimulus exposure. In discussing the results, Sartory et al. three keywords were used to refine the results generated. The first
highlight that participants with PTSD showed significantly more of the keywords included one of the following: “traumatic memory
common brain activation in the precuneus, restrosplenial cortex, reexperiencing,” “traumatic memory retrieval,” “traumatic memory
caudate nucleus, and anterior cingulate as compared with controls. reliving,” “autobiographical memory recall,” “autobiographical reex-
By contrast, trauma‐exposed controls displayed more consistent periencing,” “autobiographical memory,” “autobiographical memory
activation in the superior temporal, middle occipital, and post- testing,” “script‐driven imagery,” “symptom provocation,” or “mental
central gyri as compared with PTSD. Notably, participants with imagery.” These keywords were then combined with either “post-
PTSD showed more common activation of regions often implicated traumatic stress disorder” or “PTSD.” The last keyword included
in re‐experiencing symptoms (i.e., precuneus, restrosplenial cor- either “functional magnetic resonance imaging” or “fMRI” (for the
tex), which is corroborative with the altered trauma‐related AM combination breakdown, see Supporting Information Materials S1).
features. Taken together, these findings support the notion that The literature search and the research abstract screening was
PTSD is associated with abnormal functioning of the AM network conducted by author J. T. Full‐text articles were assessed for
during trauma‐related AM retrieval. eligibility by authors B. T. and J. T., independently. Decision for the
The research reviewed here points strongly to the role of AM in inclusion or the exclusion of the identified studies was based on
the development of a sense of self that emerges in response to the further screening and discussion by authors R. A. L., B. T., and J. T.
dynamic interplay of episodic and of semantic memory components. Studies were included if they met the following inclusion criteria: (a)
The present study builds on the earlier findings of Sartory et al. the PTSD patient group met the diagnostic criteria as defined by the
(2013) by conducting an updated meta‐analysis examining the Diagnostic and Statistical Manual of Mental Disorders (DSM) (DSM‐
differences in brain activation during trauma‐related AM in a larger III or later); (b) participants were exposed to a paradigm that was
sample of participants with PTSD and control subjects. Moreover, associated with a trauma‐related memory (i.e., explicit exposure to a
our meta‐analysis is novel in that we conduct symptom correlations traumatic script or a trauma‐related stimulus); (c) the experimental
with reports of brain activation across the included studies. In contrast included trauma‐related AM recollection or provocation of
addition, we employ two meta‐analytic methods (i.e., activation trauma‐related AMs as compared with another condition (i.e.,
likelihood estimation, effect‐size signed differential mapping) to neutral/negative script, neutral/negative words, neutral/negative
assess convergence across the meta‐analytic approaches and per- sounds/images), or to a baseline condition; (d) the contrasts were
form sensitivity estimations to determine the robustness of the reported as either within‐group or between‐group comparisons. The
findings. Finally, in the present meta‐analysis, we distinguish between between‐group comparisons had to include either a healthy,
THOME ET AL. | 5
F I G U R E 1 Flowchart of fMRI study inclusion and exclusion process for the meta‐analysis of trauma‐related AM retrieval and/or
re‐experiencing in posttraumatic stress disorder. Abbreviations: AM, autobiographical memory; fMRI, functional magnetic resonance imaging
nontrauma‐exposed or a healthy, trauma‐exposed control sample. emphasize the aspect that their study design operationalizes
Additionally, studies were included if within‐group symptom correla- re‐experiencing (e.g., Bremner, Narayan, et al., 1999; Dahlgren
tions within the PTSD sample were reported; and (e) whole‐brain or et al., 2018; Lanius et al., 2001; Shin et al., 2004) (see also,
region‐of‐interest (ROI) results were reported with associated St Jacques et al., 2011). Hence, studies examining the response
stereotactic coordinates. In case of publications reporting analyses during AM stimulus presentation are thought to capture mainly the
on a similar or an overlapping sample, only the most recent retrieval of a given AM (Botzung et al., 2008; St Jacques et al., 2011).
publication was included (exclusion: Cisler et al., 2014; Hou et al., However, the distinction is not always confirmed by further analysis
2007; Ke et al., 2015). Included publications were then cross‐checked (i.e., subjective experiences).
for additional references that may have been missed. Moreover, we Nineteen of these studies reported within‐group findings in their
compared the identified studies to a previous meta‐analysis on PTSD sample (retrieval: N = 11; re‐experiencing: N = 8), and eight
trauma‐related AM in PTSD as conducted by Sartory et al. (2013). studies reported within‐group findings in their control sample
Studies that were reported by Sartory et al. but not identified based (retrieval: N = 5; re‐experiencing: N = 3). Twelve studies contributed
on our search criteria were included to the meta‐analyses (i.e., between‐group analyses of PTSD as compared with a control group
Bremner, Narayan, et al., 1999; Bremner, Staib, et al., 1999; Driessen (PTSD > Controls: retrieval: N = 9; re‐experiencing: N = 3; controls >
et al., 2004; Flatten et al., 2004; Liberzon et al., 1999; Morey et al., PTSD: retrieval: N = 6; re‐experiencing: N = 6). Notably, four of the
2009; Pissiota et al., 2002; Rauch et al., 1996; Shin et al., 1997, 1999). between‐group comparisons included healthy, nontrauma‐exposed
In total, twenty‐eight studies met the inclusion criteria for the controls as opposed to trauma‐exposed control subjects. The
meta‐analysis (see Tables 1A and Figure 1). The assignment of between‐group meta‐analyses were thus re‐run after removal of
studies to the category of “retrieval” or “reexperiencing” was based the four studies reporting the between‐group comparisons with
on whether the study focused on the neural response during or after healthy, nontrauma‐exposed controls and are included in the
trauma‐related stimulus exposure. Here, the rational is rooted in the Supporting Information (Tables S2 and S4; PTSD > trauma‐exposed
fact that studies focusing on the response post‐AM cue exposure did controls: retrieval: N = 5; trauma‐exposed controls > PTSD: retrieval:
6
|
T A B L E 1A fMRI studies on trauma‐related AM in PTSD: Sample and paradigm description
PTSD Controls
Studies Year N N Type Paradigm Stimulus duration Stimulus order Time course of interest Contrast of interest
Bremner et al. 1999 10 12 TEC Script‐driven imagery 60 s Fixed (neutral first) During and 20 s after stimulus Trauma script > neutral
presentation
Bremner et al. 1999 10 10 TEC Trauma‐related/neutral Four pictures in 120 s Fixed (neutral first) During stimulus presentation Trauma > neutral
pictures
Britton et al. 2005 16 15 TEC Script‐driven imagery 40 s Randomized After stim/25 s overlap Trauma script > neutral
Cwik et al. 2017 19 None TEC Trauma‐related/neutral 3–5 s n.a. During stimulus presentation Trauma > neutral pictures
pictures
Dahlgren et al. 2018 12 14 TEC Script‐driven imagery 50 s n.a. After stimpres/duration 30 s Trauma script > neutral
Driessen et al. 2004 6 6 TEC Script‐driven imagery n.a. Randomized After stimpres/duration 30 s Trauma script > neutral
Hopper et al. 2007 27 None None Script‐driven imagery 30 s n.a. After stimpres/duration 30 s Trauma script > neutral
Ke et al. 2016 12 14 TEC Trauma‐related/baseline 6s Fixed (neutral first) During stimulus presentation Trauma script > baseline
pictures
Landre et al. 2012 17 17 HC Trauma‐related/neutral 2s Randomized During stimulus presentation Trauma > neutral words
words
Lanius et al. 2001 9 9 TEC Script‐driven imagery 30 s Fixed After stimpres/duration 30 s Trauma script > baseline
Lanius et al. 2003 10 10 TEC Script‐driven imagery 30 s Fixed (neutral first) After stimpres/duration 30 s Trauma script > baseline
Liberzon et al. 1999 14 11 TEC Trauma‐related/neutral 180 s Fixed During stimulus presentation Trauma > neutral sounds
sounds
Ludäscher et al. 2010 15 None none Script‐driven imagery 25–32 s Fixed (neutral first) During stimulus presentation Trauma script > neutral
Mickleborough et al. 2011 17 26 TEC Pain during script‐driven 30 s Fixed (neutral first) After stimpres Trauma script > neutral
imagery
Morey et al. 2008 39 None None Trauma‐related/neutral 2s Fixed (neutral first) During stimulus presentation Trauma > neutral pictures
pictures
Piefke et al. 2008 6 None None Script‐driven imagery 90 s Fixed (stress,trauma,neutral) During stimulus presentation Trauma script > baseline
Pissiota et al. 2002 7 None None Trauma‐related/neutral n.a. Fixed (neutral first) During stimulus presentation Trauma > neutral sounds
sounds
Protopopescu et al. 2005 9 14 HC Trauma‐related/panic‐ 2s Randomized During stimulus presentation Trauma > neutral words
related/
Positive/neutral words
Rabellino et al. 2016 26 20 HC Subliminal and 16 ms Fixed During stimulus presentation Trauma > neutral words
supraliminal
Trauma‐related/neutral
words +
Fearful/neutral faces
THOME
Rauch et al. 1996 8 None None Script‐driven imagery n.a. Randomized After stimpres/duration 90 s Trauma script > neutral
ET AL.
(Continues)
THOME ET AL. | 7
N = 5; note that none of the “reexperiencing” studies included a
Abbreviations: fMRI, functional magnetic resonance imaging; HC, nontrauma‐exposed, healthy controls; PTSD, posttraumatic stress disorder; stimpres, stimulus presentation; TEC, trauma‐exposed, healthy
Trauma > negative scenes
nontrauma‐exposed control group). Seven studies contributed
Trauma script > negative

Trauma > neutral words
After stimpres/delay 30 s/duration Trauma script > neutral
After stimpres/delay 30 s/duration Trauma script > neutral
Trauma script > neutral

within‐group positive correlations of PTSD symptom severity and
Contrast of interest brain activation during trauma‐related AM (retrieval: N = 5; re‐
experiencing: N = 2). PTSD symptom severity was assessed either by
the Clinician Administered PTSD Scale (CAPS; Blake et al., 1990),
Davidson Trauma Scale (DTS; Davidson, Tharwani, & Connor, 2002),
or the Posttraumatic Symptom Scale (PSS; Falsetti, Resnick, Resick, &
Kilpatrick, 1993). However, we did not run a quantitative analysis for
During stimulus presentation

After stimulus presentation/
negative correlations of PTSD symptom severity and common brain

activation, or for correlations with other PTSD‐relevant symptoms in
Time course of interest
duration self‐paced
general (i.e., dissociation, anxiety), as only a few studies were

identified to report on these correlations. Nevertheless, these
findings are summarized descriptively in the Tables S5–S7 as well
as Figures S1 and S2.
60 s
60 s
2.2 | Experimental contrast selection

The present investigation focused on trauma‐related AM. To this end,
Fixed (neutral first)
we were interested in both the voluntary retrieval and the

Stimulus order
subsequent re‐experiencing of the trauma‐related AM as well as

Randomized
Randomized
Randomized
studies employing trauma‐related material to evoke traumatic

AMs in participants with PTSD as well as in nontrauma‐ and
Fixed
n.a.
trauma‐exposed controls. Hence, reported common brain activation

may not be driven primarily through the explicit and thus the verbal
Stimulus duration
retrieval and re‐experiencing of a trauma memory, but rather also

reflect the implicit retrieval and re‐experiencing of the memory
following exposure to an associated trauma‐related cue or stimulus.
1–1.7 s
.033 s
Trauma‐related material included trauma‐related AM scripts as

n.a.
n.a.
n.a.
6s
well as trauma‐related stimuli (i.e., words, images, sounds), which

were in contrast to a neutral or a negative AM script as well as a
Trauma‐related/negative
Trauma‐related/negative
Trauma‐related/flower
Script‐driven imagery
neutral or a negative stimulus, or to a baseline condition in a few

cases (see Tables 1A and 1B).
Findings based on whole‐brain (N = 22), as well as ROI analyses
Paradigm
pictures
pictures
pictures
(N = 6) were included in the current analyses. Activation foci of the

contrast of interest were extracted (i.e., peak coordinates and their
respective T values and Z values) for each study. Individual meta‐
analyses were run separately for the following contrasts, and for
Type
none
TEC
TEC
TEC
TEC
HC
each category namely: (a) across all identified studies (i.e., retrieval
Controls
and re‐experiencing), (b) studies categorized as specific to trauma‐

None
related AM retrieval, and (c) studies categorized as specific to

16
19
24
26
N
trauma‐related AM re‐experiencing; where each of the identified

PTSD
studies was represented only once in each meta‐analysis to avoid

16
16
17
10
38
N
presenting more than one contrast that matched inclusion criteria: (a)
2005
1997
1999
2004
2013
2011
Year
within PTSD, (b) within controls, (c) PTSD > control, (d) control >
PTSD, and (e) within PTSD symptom correlations. For a meta‐analysis
(Continued)
conducted on the differences between participants with PTSD as

compared with healthy, trauma‐exposed controls see Supporting
Information (see Tables S2 and S4). In the case of a study presenting
Sakamoto et al.
Whalley et al.
more than one contrast that matched our inclusion criteria (i.e.,
TABLE 1A
Zhang et al.
Shin et al.
Shin et al.
Shin et al.
trauma vs. neutral and trauma vs. baseline condition), we selected the
Studies
controls.
control condition that was most alike to the experimental condition

of interest, that is e.g., neutral condition as oppose to a baseline
8 | THOME ET AL.
T A B L E 1B fMRI studies on trauma‐related AM in PTSD: Analysis approach and contrast description
Contrast reported
Within Between
Studies Analysis Type p PTSD Controls Symptoms PTSD > Controls >
Bremner WB uncorr .001 1 1 0 1 1
Bremner WB uncorr .001 1 1 0 1 1
Britton WB uncorr .005 1 1 0 0 0
Cwik WB uncorr .005 0 0 1† 0 0
Dahlgren WB corr .001 0 0 0 0 1
Driessen WB corr .05 1 0 0 0 0
a
Hopper ROI corr .05 1 0 1 0 0
†
Ke WB corr .05 0 0 1 1 1
Landre WB corr .005 1 1 0 1 0
Lanius WB uncorr .001 0 0 0 0 1
Lanius WB corr .05 0 0 0 1 1
Lanius WB corr .05 0 0 0 0 1
Lanius SVC corr .05 1 1 0 1 1
Liberzon WB corr .05 1 1 0 0 0
Ludäscher WB uncorr .001 1 0 0 0 0
†,a
Mickleborough ROI corr .001 1 0 1 1 0
†
Morey WB corr .05 1 0 1 0 0
Piefke ROI corr .01 1 0 0 0 0
Pissiota WB corr .01 1 0 0 0 0
Protopopescu SVC uncorr .001 0 0 1† 1 0
Rabellino ROI corr .001 1 0 1† 1 0
Rauch WB uncorr .001 1 0 0 0 0
a
Sakamoto WB uncorr .001 1 1 1 1 1
Shin WB uncorr .001 1 1 0 0 0
Shin WB uncorr .001 1 0 0 0 0
Shin WB uncorr .001 1^ 0 1† 1^ 1
Whalley WB uncorr .001 1 0 0 1 1
Zhang WB uncorr .001 0 0 0 1 1
Abbreviations: 1, yes; 0, no; corr, α‐level adjusted for multiple comparisons (FWE or FDR); fMRI, functional magnetic resonance imaging;
PTSD, posttraumatic stress disorder; ROI, region‐of‐interest analysis; SVC, small volume correction; uncorr, α‐level not adjusted for multiple comparisons;
WB, whole‐brain analysis.
†
Symptom correlations.
^
Contrast reported could not be included in present analyses, as analyses has been conducted across PTSD and control subjects.
a
Descriptive presentation can be found in Tables S5–S7 and Figures S1 and S2.
condition. This decision was based on the fact that a neutral paper performed five separate meta‐analyses for each of: (a) common
condition (e.g., neutral picture, word, or sound) was more comparable neural activation for trauma‐related AM in general, (b) studies
to the trauma condition in terms of the stimulus modality (e.g., visual focusing on retrieval of trauma‐related AM, and (c) studies focusing
or auditory stimulus complexity), hence the stimuli differed only in on re‐experiencing of trauma‐related AM.
regard to the content or affective nature of the material (i.e., trauma‐ The meta‐analyses included: (a) a within‐group analysis of
related vs. neutral). individuals with PTSD, (b) a within‐group analysis of control subjects
with and without trauma exposure, (c) a between‐group analysis of
brain regions displaying greater common activation in PTSD as
2.3 | Statistical analyses
compared with control subjects (i.e., PTSD > Controls), (d) a between‐
To investigate common neural activation during trauma‐related AM group analysis of brain regions displaying greater common
in participants with PTSD as well as control subjects, the present activation in controls as compared with participants with PTSD
THOME ET AL. | 9
(i.e., Control > PTSD), and (e) a within‐group positive correlation of event that an effect size was not reported in the primary study, the
PTSD symptom severity scores (i.e., CAPS, DTS, PTSS) and common direction of the finding (i.e., activation or deactivation) was used to
brain activation as reported in the PTSD patient sample across the calculate the minimum effect size. Coordinates reported in
included studies. Talairach space were converted to Montreal Neurological Institute
As mentioned, four studies reported analyses on negative (MNI) space via Lancaster transformation (incorporated within the
correlations of PTSD symptom severity, while two studies performed ES‐SDM software). Preprocessing of the incorporated peaks (i.e.,
correlations with state dissociation during trauma‐related AM. activation foci) involved smoothing as described before (anisotropic
However, due to the small number of these reported studies, we kernel of 20 mm full‐with at half maximum; Radua et al., 2014). The
did not perform a quantitative meta‐analysis on negative correlations created study maps were subsequently used to calculate random‐
of PTSD symptom severity or state dissociation and brain activation effects models, taking the sample size and intra‐ as well as
during trauma‐related AM. Nevertheless, we provide descriptive interstudy variance into account. Statistical significance was
information on these correlations within the Supporting Information determined using the randomization test (50 permutations). Results
(see Tables S5–S7 and Figures S1 and S2; negative correlation PTSD are reported that survived a standard thresholding of an SDM Z
symptom severity: Cwik et al., 2017; Ke et al., 2016; Mickleborough value ≥ 1, a voxel height threshold of 1, a peak probability of
et al., 2011; Rabellino, Densmore, Frewen, Theberge, & Lanius, 2016; p ≤ .005, with a cluster extent threshold of ≥20 (Radua et al., 2012;
other symptoms: Hopper et al., 2007; Sakamoto et al., 2005). see also Hart, Radua, Mataix‐Cols, & Rubia, 2012; Sartory et al.,
To test the replicability of the meta‐analysis conducted by 2013; Schulze, Schmahl, & Niedtfeld, 2016; Schulze, Schulze,
Sartory et al. (2013), we performed a coordinate‐based meta‐analysis Renneberg, Schmahl, & Niedtfeld, 2019). Robustness of the findings
with the effect‐size signed differential mapping software (ES‐SDM was analyzed by a jackknife analysis, i.e., data from one contrast (i.e.,
instead; version 5.142; http://www.sdmproject/com; Radua et al., study) is removed systematically from the analysis to determine if
2012, 2014). In addition, meta‐analyses were also repeated through the results remain significant. The process is repeated for all
application of the widely applied activation‐likelihood estimation possible combinations to estimate the robustness of the findings as
(ALE) technique (Eickhoff et al., 2009; Turkeltaub, Eden, Jones, & derived from the persistence of significant thresholds met, while
Zeffiro, 2002), as implemented using version 2.3.6 of the GingerALE also permitting authors to determine if certain results are driven
software (http://www.brainmap.org/ale). Both methods have in predominantly by a small set of studies.
common that they convolve a kernel with each included peak
coordinate (i.e., activation foci) (for a description see Radua et al.,
2.3.2 | Activation‐likelihood estimation
2012, 2014). Here, “kernel” means that an effect size (effect‐size
signed differential mapping [ES‐SDM]) or a likelihood (ALE) is The ALE method involves extracting the activation foci from
assigned to each voxel, roughly based on its Euclidean distance to individual studies, converted into Talairach space (spm MNI to
its closest peak (i.e., activation foci) by means of an (un)normalized TAL function), which are, in turn, smoothed as previously described,
Gaussian kernel, respectively (e.g., Radua et al., 2012, 2014). First taking the full‐width at half maximum threshold for each distribu-
versions of the ES‐SDM algorithms further multiplied the kernel with tion, while taking its sample size into account (i.e., likelihood map for
the effect size of a given voxel (in case of more than one assigned each peak). The ALE method considers the threshold of each
peak, these values were averaged weighting by the square of the distribution as well as the sample size of the study to produce a
distance to the closest peaks; Radua et al., 2012). The new ES‐SDM likelihood map. Likelihood maps are generated for each study and
method contrarily is based on the idea that voxels close to each other then combined to estimate the probability of union in the meta‐
are more likely to correlate higher, meaning that higher correlated analysis. Results are reported that survive a threshold of un-
voxels are assumed to lie closer together. Based heron, the distance corrected p ≤ .001
between voxels is “rearranged,” bringing voxels closer together that
are highly correlated, while uncorrelated voxels are moved further
away. The Gaussian kernel is then applied to this new deformed 3 | RESULTS
space and subsequently, voxels are restored in their original space
(Radua et al., 2014). In total, twenty‐eight study samples were included that investigated
414 participants with PTSD as well as 296 control subjects (trauma‐
exposed: N = 229; healthy, nontrauma‐exposed: N = 67). The follow-
2.3.1 | Effect‐size signed differential mapping
ing results pertain to common neural activation across these groups
In general, the ES‐SDM technique considers the activation peaks’ during trauma‐related AM recollection, as estimated by the ES‐SDM
effect sizes, while also weighting the studies by intrastudy variance technique. Findings were reported that survived a thresholding
and interstudy heterogeneity (Radua et al., 2012). For all criterion of an SDM Z value ≥ 1, a voxel height threshold of 1, a peak
coordinate‐based results, peaks, and their associated Z or T values probability of p ≤ .005, with a cluster extent threshold of ≥20.
were extracted from whole‐brain and ROI‐related reports by Findings for each particular analysis are listed in order of descending
authors B. T. and J. T., independently and cross‐checked. In the robustness, as defined by the jackknife analysis described above.
10 | THOME ET AL.
T A B L E 2 Brain regions recruited most commonly within studies on trauma‐related AM: (a) retrieval and re‐experiencing, (b) retrieval, and (c)
re‐experiencing in participants with PTSD and control subjects (ES‐SDM meta‐analysis)
Peak
MNI coordinates Cluster
Contrast R/L Brain region x y z SDM‐Z p Size BA Jackknife

(a) Retrieval + re‐experiencing
Controls within R Ventromedial/dorsomedial PFC 2 46 −4 1.52 .001 470 9/10/24/32 6/8
Perigenual anterior cingulate cortex
R Posterior cerebellar lobule VI 8 −76 −18 1.43 .003 76 6/8
L Lingual gyrus/inferior/middle occipital lobe −30 −86 −14 1.74 .003 987 18/19 2/8
PTSD within L Precentral gyrus −50 4 32 2.50 <.001 264 6/9 19/19
L Caudate nucleus −6 6 4 2.48 <.001 362 18/19
R Ventromedial/dorsomedial prefrontal 6 54 2 2.65 <.001 660 9/10 17/19
cortex
L Angular gyrus/inferior parietal cortex −54 −52 32 2.03 .003 28 39/40 16/19
R/L Dorsal anterior cingulate cortex −4 12 24 2.11 .002 52 24/33 14/19
L Temporal pole/superior temporal gyrus −48 8 −8 2.13 .002 107 22/48 13/19
R Insula 50 2 0 2.33 <.001 722 13/48 13/19
Controls > R Ventromedial/dorsomedial prefrontal 4 44 −10 1.96 <.001 2,558 10/11/24/25 12/12
PTSD cortex
L Midline nucleus/medial/lateral dorsal −6 −16 14 1.65 <.001 305 12/12
nucleus thalamus
L Angular gyrus −50 −72 26 1.49 .001 78 39 12/12
PTSD > controls L Posterior cingulate/precuneus/ −2 −46 32 2.59 <.001 3,732 7/23/24/30/ 12/12
midcingulate cortex 31/32
R Parahippocampal gyrus 18 −30 −18 1.51 .001 217 28/30/35 11/12
R Dorsal anterior cingulate cortex 14 40 14 1.51 .001 36 32 9/12
(b) Retrieval
Controls within R Ventromedial/dorsomedial prefrontal 4 48 8 1.78 <.001 1,049 9/10/24/32 4/5
cortex
R Posterior cerebellar lobule VI 8 −76 −18 1564 .001 157 3/5
PTSD within L Ventromedial frontal/perigenual anterior −2 54 −2 2.67 <.001 622 9/10/32 11/11
cingulate cortex
L Precentral gyrus −46 2 32 2.84 <.001 186 6 9/11
L Supramarginal gyrus −56 −50 26 2.36 .002 29 40 9/11
L Caudate nucleus −12 10 18 2.26 .003 26 8/11
Controls > L Middle temporal gyrus −50 −68 20 1.50 .001 224 39 5/6
PTSD R Medial orbitofrontal/perigenual anterior 16 24 −16 1.47 .001 238 11/25 4/6
cingulate cortex
PTSD > controls R Posterior cingulate/precuneus/ 2 −36 34 2.33 <.001 2,504 23 9/9
midcingulate cortex
R Parahippocampal gyrus 16 −32 −18 1.62 <.001 390 9/9
L Precentral gyrus −38 −10 44 1.38 .002 57 4/6 7/9
(c) Re‐experiencing
Controls within R Insula 44 −6 −2 1.46 <.001 26 48 3/3
PTSD within R Insula/amygdala/parahippocampal gyrus 36 −8 12 2.60 <.001 3,070 48 8/8
L Caudate nucleus/striatum −4 12 2 1.28 .003 24 7/8
R Medial frontal gyrus 14 50 6 1.72 <.001 44 9/10 6/8
Controls > R Ventromedial/dorsomedial prefrontal 4 44 0 2.60 <.001 3,832 10/11/12/24/ 6/6
PTSD cortex 32
L Midline nucleus/medial/lateral dorsal −2 −14 16 1.77 <.001 544 4/6
nucleus thalamus
R Inferior frontal gyrus 46 34 −6 1.54 .001 293 47 4/6
R Precuneus 28 −82 44 1.63 <.001 127 19 4/6
L Dorsal anterior cingulate cortex −2 −2 28 1.51 .001 186 24 2/6
(Continues)
THOME ET AL. | 11
TABLE 2 (Continued)
Peak
MNI coordinates Cluster

PTSD > controls R Caudate nucleus 8 16 6 1.95 <.001 345 25 3/3
L Posterior cingulate/precuneus −4 −62 −26 1.64 <.001 1,682 23 1/3
R Dorsal anterior cingulate cortex 4 16 22 1.84 <.001 1,230 24 1/3
R Ventromedial prefrontal gyrus 6 58 4 1.29 .003 75 10 1/3
R Middle temporal gyrus 52 −72 28 1.33 .002 35 39 0/3
Note: Results thresholded at a SDM Z value ≥ 1, a voxel height threshold of 1, a peak probability of p ≤ .005, and a cluster extent threshold of ≥20.
Abbreviations: BA, Brodmann Area; L, left; MNI, Montreal Neurological Institute coordinates; PTSD, posttraumatic stress disorder; R, right; SDM‐Z,
effect‐size signed differential mapping Z value.
Findings of the ALE methods are reported in the Supporting (extending into the orbitofrontal and the perigenual anterior
Information (for within‐ and between‐group differences, see Tables cingulate) (BA 10, 11, 24, 25), the left midline nucleus of the
S1 and S2; positive PTSD symptom correlations, see Table S3; Figure 1). thalamus (extending into the medial and the lateral dorsal nuclei),
and the left angular gyrus (BA 39) (see Table 2a and Figure 3). The
3.1 | Trauma‐related AM recollection (i.e., retrieval results did not change after excluding studies comparing nontrauma‐
and re‐experiencing) exposed controls to participants with PTSD (see Table S4).
3.1.1 | Controls: Within‐group trauma‐related AM

3.1.4 | PTSD > Control: Between‐group comparison
In controls, a combined meta‐analysis across all identified studies on
of trauma‐related AM
trauma‐related AM recollection (i.e., retrieval and re‐experiencing;
N = 8) revealed common neural activation with the most robust findings In comparing neural activation during trauma‐related AM between
in clusters centered on the right ventromedial orbitofrontal gyrus groups (i.e., retrieval and re‐experiencing; N = 12), as compared with
(extending into the dorsomedial prefrontal and the perigenual anterior controls, individuals with PTSD displayed more common neural activation
cingulate) (BA 9, 10, 24, 32), and the cerebellar posterior lobule VI. in a cluster centered on the left posterior cingulate (extending into
Controls also displayed common neural activation of the left lingual the precuneus and the mid‐cingulate cortex) (BA 7, 23, 24, 30, 31, 32) and
gyrus (extending into the inferior and the middle occipital lobe), where the right parahippocampal gyrus (BA 28, 30, 35). Moreover, in PTSD,
this finding is less robust (BA 18, 19) (see Table 2a and Figure 2). more common activation was observed in the right dorsal anterior
cingulate cortex (BA 32) as compared with controls, whereby this finding
is found to be less robust (see Table 2a and Figure 3). Results did not
3.1.2 | PTSD: Within‐group trauma‐related AM
change after excluding studies comparing nontrauma‐exposed controls to
In PTSD, a combined meta‐analysis across all identified studies on participants with PTSD (see Table S4).
trauma‐related AM recollection (i.e., retrieval and re‐experiencing;
N = 19) revealed common neural activation with the most robust
3.1.5 | PTSD symptom severity and its relation to
findings in clusters centered on the left precentral gyrus (BA 6,9), the
trauma‐related AM
left caudate nucleus, and the right ventromedial prefrontal gyrus
(extending into the dorsomedial prefrontal cortices) (BA 9, 10). A meta‐analysis on PTSD symptom severity (i.e., CAPS, DTS, PSS
Common neural activation was also revealed for the left angular total scores; N = 7) revealed that PTSD symptom scores were
gyrus (extending into the inferior parietal cortices) (BA 39, 40), the associated positively with common neural activation during trauma‐
bilateral dorsal anterior cingulate (BA 24, 33), the left temporal pole related AM (i.e., retrieval and re‐experiencing) in clusters centered on
(extending into the superior temporal gyrus) (BA 22, 48), and the the left insula (extending into the lentiform nuclei, the putamen, the
right insula (BA 13, 48), whereby these findings are listed in order of hippocampus, and the amygdala) (BA 13, 48), the right caudate
descending robustness (see Table 2a and Figure 2). nucleus (extending into the thalamic anterior nucleus), and the right
middle frontal gyrus (BA 9, 10, 45). Moreover, PTSD symptom
severity was also correlated positively with common neural activa-
3.1.3 | Control > PTSD: Between‐group comparison
tion in a cluster centered on the bilateral ventromedial prefrontal
of trauma‐related AM
gyrus (extending into the perigenual anterior cingulate) (BA 9, 10, 11,
In comparing neural activation during trauma‐related AM between 24, 32), whereby this finding is less robust than the former
groups (i.e., retrieval and re‐experiencing; N = 12), as compared with (see Table 3a and Figure 4). For a descriptive overview of the
PTSD, control subjects exhibited more common neural activation in negative correlations between PTSD symptom scores and trauma‐
clusters centered on the right ventromedial prefrontal cortex related AM, see Table S5 and Figure S1 (Figure 5).
12 | THOME ET AL.
F I G U R E 2 Within‐group findings of common neural activation for: (a/b) control subjects and (c/d) participants with PTSD (ES‐SDM
meta‐analysis). (a/c) Meta‐analytic findings across trauma‐related AM retrieval and re‐experiencing. (b/d) Meta‐analytic findings on AM retrieval (lighter
color), and re‐experiencing (darker color). Results are thresholded at: SDM Z value ≥ 1, a voxel height threshold of 1, a peak probability of p ≤ .005, with a
cluster extent threshold of ≥20. Abbreviations: dACC, dorsal anterior cingulate cortex; dm, dorsomedial; inf, inferior; mid, middle; PFC, prefrontal cortex;
pHG, parahippocampal gyrus; PTSD, posttraumatic stress disorder; STG, superior temporal gyrus; vm, ventromedial
3.2 | Trauma‐related AM retrieval cluster centered on the right ventromedial prefrontal cortex
(extending into the dorsomedial prefrontal and the perigenual
anterior cingulate cortex) (BA 9, 10, 24, 32). Common neural
retrieval
activation was also observed in the left lingual gyrus (BA 18,19)
In controls, a meta‐analysis on trauma‐related AM retrieval (N = 5) and the right posterior cerebellum lobule VI in control subjects (see
revealed common neural activation with the most robust finding in a Table 2b and Figure 2).
THOME ET AL. | 13
F I G U R E 3 Between‐group findings of common neural activation between participants with PTSD as compared with control subjects
(ES‐SDM meta‐analysis). (a) Meta‐analytic findings across all identified studies. (b) Meta‐analytic findings on trauma‐related AM retrieval.
(c) Meta‐analytic findings on trauma‐related AM re‐experiencing. Results are thresholded at SDM Z value ≥ 1, a voxel height threshold of
1, a peak probability of p ≤ .005, with a cluster extent threshold of ≥20. Abbreviations: dACC, dorsal anterior cingulate cortex; MidNuc,
midline nucleus (thalamus); MiTG, middle temporal gyrus; (i)OFC, (inferior)orbitofrontal cortex; pACC, perigenual anterior cingulate
cortex; PCC, posterior cingulate cortex; pHG, parahippocampal gyrus; PTSD, posttraumatic stress disorder; vmPFC, ventromedial
prefrontal cortex
3.2.2 | PTSD: Within‐group trauma‐related AM 3.2.3 | Control > PTSD: Between‐group comparison
retrieval of trauma‐related AM retrieval
In participants with PTSD, a meta‐analysis on trauma‐related AM In comparing neural activation during trauma‐related AM retrieval
retrieval (N = 11) revealed common neural activation with the between groups (N = 6), as compared with PTSD, controls exhibited
most robust findings associated with clusters centered on the significantly more common neural activation in the left middle
left ventromedial prefrontal cortex (extending into the perigen- temporal gyrus (BA 39) as well as the right medial orbitofrontal
ual anterior cingulate cortex) (BA 9, 10, 32), the left precentral cortex (extending into the perigenual anterior cingulate cortex) (BA
gyrus (BA 6), the left supramarginal gyrus (BA 49), and the left 11, 25) (see Table 2b and Figure 3). The results did not change after
caudate nucleus of the dorsal striatum (see Table 2b and excluding studies comparing nontrauma‐exposed control subjects to
Figure 2). participants with PTSD (see Table S4).
14 | THOME ET AL.
T A B L E 3 Common brain regions associated positively with PTSD symptom severity during trauma‐related AM across studies on: (a) retrieval
and re‐experiencing, and (b) retrieval in participants with PTSD (ES‐SDM meta‐analysis)
Peak Cluster
MNI coordinates

(a) Retrieval + re‐experiencing
L Insula/lenticular nucleus/putamen/hippocamus/ −28 2 −6 3.53 <.001 1262 13/48 7/7
amygdala
R Caudate nucleus/anterior nucleus thalamus 6 10 8 3.25 <.001 590 6/7
R Middle frontal gyrus 40 42 20 2.14 .002 90 9/10/45 5/7
R/L Ventromedial prefrontal/perigenual anterior −8 38 −10 3.00 <.001 1863 9/10/11/24/32 4/7
cingulate cortex
(b) Retrieval
R/L Ventromedial prefrontal/perigenual anterior −10 48 −8 3.58 <.001 2207 9/10/11/24/32 5/5
cingulate cortex
L Insula/lenticular nucleus/putamen/hippocamus/ −26 2 −8 3.63 <.001 1205 13/48 4/5
amygdala
R Middle frontal gyrus 42 40 22 2.34 .001 171 9/10/45 4/5
R Caudate nucleus/anterior nucleus thalamus 8 10 4 2.95 <.001 579 3/5
Note: Results are thresholded at: SDM Z value ≥ 1, a voxel height threshold of 1, a peak probability of p ≤ .005, with a cluster extent threshold of ≥20;
PTSD symptoms as assessed with either the CAPS, DTS, or PTSS.
Abbreviations: BA, Brodmann Area; CAPS, Clinician Administered PTSD Scale; DTS, Davidson Trauma Scale; L, left; MNI, Montreal Neurological Institute
coordinates; PTSD, posttraumatic stress disorder; R, right; SDM‐Z, effect‐size signed differential mapping Z value.
3.2.4 | PTSD > Control: Between‐Group comparison 3.2.5 | PTSD symptom severity and its relation to
of trauma‐related AM retrieval trauma‐related AM retrieval
In comparing neural activation during trauma‐related AM retrieval A meta‐analysis on PTSD symptom severity (i.e., CAPS, DTS, PSS
between groups (N = 9), as compared with controls, PTSD displayed scores; N = 7) revealed that PTSD symptom scores were correlated
more common activation in clusters centered on the left posterior positively with common neural activation during trauma‐related AM
cingulate (extending into the precuneus and the mid‐cingulate gyrus) retrieval in clusters centered on the left superior frontal gyrus
(BA 7, 23, 24, 30, 31, 32), the right parahippocampal gyrus (BA 28, 30, (extending into the medial orbitofrontal gyrus) (BA 10), the left insula
35), and the left precentral gyrus (BA 4, 6) (see Table 2b and Figure 3). (extending into the lenticular nucleus, the putamen, the hippocampus,
The results did not change after excluding studies comparing and the amygdala) (BA 48), the right middle frontal gyrus (BA 45), and
nontrauma‐exposed control subjects to participants with PTSD (see the right caudate nucleus (extending into the anterior nucleus of the
Table S4). thalamus) (see Table 3b and Figure 4).
F I G U R E 4 Positive association between PTSD symptom severity and brain activation during trauma‐related AM in PTSD (ES‐SDM meta‐analysis).
Figure displays meta‐analytic findings across all studies. Results did not change when conducting the meta‐analysis on retrieval studies solely. A meta‐
analysis on studies focusing on re‐experiencing solely was not conducted due to the small number of studies available. Results are thresholded at
SDM Z value ≥ 1, a voxel height threshold of 1, a peak probability of p ≤ .005, with a cluster extent threshold f ≥ 20. Abbreviations: AntNuc, anterior
nucleus (thalamus); lenNuc, lentiform nucleus; MiFG, middle frontal gyrus; pACC, perigenual anterior cingulate cortex; PCC, posterior cingulate
cortex; PTSD, posttraumatic stress disorder; vmPFC, ventromedial prefrontal cortex
THOME ET AL. | 15
frontal gyrus (BA 47), and the right precuneus (BA 19). Moreover, in
controls as compared with PTSD, more common activation was observed
in the dorsal anterior cingulate, where this finding is less robust (see
Table 2c and Figure 3). Since only healthy, trauma‐exposed subjects have
been compared with PTSD across all the included studies, these analyses
were not repeated.
3.3.4 | PTSD > Control: Between‐group comparison

of trauma‐related AM re‐experiencing
In comparing the neural activation during trauma‐related AM re‐
experiencing between groups (N = 3), as compared with controls, PTSD
F I G U R E 5 Summary of the key findings of the meta‐analysis on displayed more common neural activation in the right caudate nucleus.
trauma‐related AM in PTSD. Figure displays illustratively the AM Moreover, in PTSD, more common activation was observed in a cluster
network (displayed masks taken from https://findlab.stanford.edu/ centered on the left posterior cingulate cortex (extending into the
functional_ROIs.html) and its stronger recruitment in PTSD versus
precuneus) (BA 23), the right dorsal anterior cingulate cortex (BA 24), the
controls across all identified studies (i.e., re‐experiencing and
right ventromedial prefrontal cortex (BA 10), and the right middle
retrieval). Brain regions that have been not identified as being more
commonly activated in PTSD or controls during trauma‐related AM temporal gyrus (BA 39) as compared with controls, where these findings
are displayed in light blue. Abbreviations: AM, autobiographical are listed in order of descending robustness (see Table 2c and Figure 3).
memory; PTSD, posttraumatic stress disorder Since participants with PTSD were compared with healthy, trauma‐
exposed controls in all included studies, these analyses were not
repeated. Due to the limited number of included studies, these findings
3.3 | Trauma‐related AM re‐experiencing have to be interpreted with caution.

re‐experiencing 3.3.5 | PTSD symptom severity and its relation to
In controls, the meta‐analysis on trauma‐related AM re‐experiencing trauma‐related AM re‐experiencing
(N = 3) revealed common neural activation with the most robust Only two studies investigated trauma‐related AM re‐experiencing
finding in a cluster centered on the right insula (BA 48). Common with PTSD symptom severity correlations. Due to the small number
neural activation was also observed in the left lingual gyrus, where of studies, we did not run a separate meta‐analysis for this contrast.
this finding is less robust (BA 18, 19). Due to the limited number of
studies, these results are to be interpreted with caution.
4 | D I S C U SS I O N
3.3.2 | PTSD: Within‐group trauma‐related AM 4.1 | Overview

re‐experiencing
Autobiographical memory (AM) refers to the conscious recollection
In PTSD, a meta‐analysis on trauma‐related AM re‐experiencing of our personal past as derived from the interaction of multiple
(N = 8) revealed common neural activation with the most robust memory systems (Baddeley, 1992; Brewer, 1986; Rubin, 2005;
findings in clusters centered on the right insula (extending into the Svoboda et al., 2006). On a neural level, AM is facilitated by the AM
amygdala and the parahippocampal gyrus) (BA 48), the left caudate network, a distributed brain network that integrates explicit
nucleus (extending into the striatum), and the right medial frontal memory components to support the recollection of these personal
gyrus (BA 9, 10) (see Table 2c and Figure 2). memories and to provide a framework for an emergent sense of self
(Conway & Pleydell‐Pearce, 2000; Levine et al., 2002). Critically, the
AM network is shown to display altered common brain activation
3.3.3 | Control > PTSD: Between‐group comparison
during the recollection of trauma‐related AMs in PTSD (Sartory
of trauma‐related AM re‐experiencing
et al., 2013). In the present study, we conducted multiple meta‐
In comparing neural activation during trauma‐related AM re‐experiencing analyses (i.e., ES‐SDM, ALE; for a review of the ALE findings, see
between groups (N = 6), as compared with the PTSD, controls exhibited Tables S1–S3) to provide a recent account of the differences that
significantly more common neural activation in a cluster centered on the are revealed within this network during trauma‐related AM.
right ventromedial prefrontal cortex (extending into the dorsomedial Moreover, we sought to investigate these differences as a function
prefrontal and the perigenual anterior cingulate cortex) (BA 10, 11, 12, of the specific process during AM recollection, distinguishing
24, 32), a cluster centered on the left midline nucleus of the thalamus between retrieval and re‐experiencing phases for the first time in
(extending into the medial and the lateral dorsal nuclei), the right inferior a meta‐analysis on a sample of participants with PTSD. Our findings
16 | THOME ET AL.
are in large part keeping with the results generated by Sartory et al. trauma‐related AM, where the memory is recollected more as a
(2013); however, we provide a more recent and in‐depth look into relived experience and less as a controlled retrieval (Brewin, 2015;
the neural differences expressed by the network during trauma‐ Ehlers, 2010; Ehlers & Clark, 2000). Interestingly, our meta‐analysis
related AM recollection. revealed a positive correlation between PTSD symptom severity and
brain activation of the medial prefrontal cortices. At first glance, this
may seem antithetical, as individuals with PTSD displaying greater
4.2 | AM network: Control > PTSD
activation of the medial prefrontal cortices also tend to have the
The meta‐analyses revealed several brain regions exhibiting more greatest symptoms. However, it is well‐established that individuals
consistent activation in control subjects as compared with with PTSD exhibiting the greatest symptom severity are more likely
individuals with PTSD during trauma‐related AM recollection, to meet the criteria for the dissociative subtype (Frewen, Zhu, &
where the term recollection is to denote analyses that collapse Lanius, 2019; Karam et al., 2014; Lanius et al., 2014; Stein et al.,
across retrieval and re‐experiencing processes of trauma‐related 2013), identified by the presence of supplementary dissociative
AM. In particular, the control group demonstrated significantly symptoms (i.e., depersonalization, derealization; APA, 2013).
more common activation of the right medial prefrontal cortices Lanius et al. (2007) have posited that the dissociative subtype
(i.e., ventromedial, dorsomedial), the right perigenual anterior displays an overmodulation of the medial prefrontal cortices directed
cingulate, the left thalamus (midline, medial, and lateral nuclei), toward the limbic system. This is in contrast to the undermodulation
and the left angular gyrus as compared with individuals with associated more strongly with the traditional symptom pattern of
PTSD during trauma‐related AM recollection. In the meta‐ PTSD (Fenster, Lebois, Ressler, & Suh, 2018; Lanius et al., 2010,
analyses specific to retrieval processes, the control group 2014, 2018). Taken together, the positive correlation between PTSD
displayed greater common activation of the middle temporal symptom severity and activation of the medial prefrontal cortices
gyrus and the medial orbitofrontal gyrus as compared with PTSD. may be driven, in part, by the presence of dissociative symptomatol-
For analyses specific to re‐experiencing, control subjects re- ogy in these participants as an attempt to detach from the
vealed greater common activation of the medial prefrontal overwhelming emotional experience associated with their trauma
cortices, the inferior frontal gyrus, the thalamus (midline, medial, memory. To this point, two studies included in the meta‐analysis
and lateral dorsal nuclei), the precuneus, and the dorsal anterior reported dissociative symptom severity scores and, of those, one
cingulate as compared with the PTSD group. study revealed a positive association between dissociative scores and
The medial prefrontal cortices are thought to facilitate the activation of the medial prefrontal cortices in participants with PTSD
constructive processes of AM, such as memory search and controlled (Hopper et al., 2007; see Table S5 and Figure S2A).
retrieval (Cabeza & St Jacques, 2007; St Jacques et al., 2011; St. In addition to the medial prefrontal cortices, the thalamus, centered
Jacques, 2012; Svoboda et al., 2006). Specifically, the ventro‐ and the on the midline nucleus and encompassing the medial and lateral dorsal
dorsomedial prefrontal cortices are proposed to monitor the process nuclei, also revealed greater activation in controls as compared with
of AM retrieval, in particular the self‐referential aspects (Amodio & PTSD. The thalamus is a subcortical structure that relays information
Frith, 2006; Gilboa, 2004). The prefrontal cortices that underlie this between different processing regions, both subcortical and cortical
monitoring are thought to differ regionally from cortices that (Posner & Petersen, 1990; Steriade & Llinás, 1988). Given its centralized
monitor the retrieval of less personal, experimental tests of memory location and ability to facilitate communication between disparate
(i.e., paired associations, item list tasks; Moscovitch & Winocur, cortices, the thalamus serves a role in high‐level functions of arousal,
2002). Experimental memory tests reveal greater activation in lateral attention, and consciousness (Posner, 1994; Schiff, 2008; Sturm et al.,
prefrontal cortices during retrieval, whereas AM elicits greater 1999; Timofeev & Steriade, 2004). These functions are engaged during
activation of medial prefrontal cortices during retrieval processes AM recollection and rely largely on the communication between the
(Gilboa, 2004; Moscovitch & Winocur, 2002). Here, Moscovitch and prefrontal and the parietal cortices, as modulated by the thalamus (Crone
Winocur (2002) suggest AM relies on a quick, intuitive, and et al., 2014; de Bourbon‐Teles et al., 2014; Scolari, Seidl‐Rathkopf, &
preconscious form of retrieval monitoring, coined as the “feeling‐of‐ Kastner, 2015). The impaired thalamic ability to transmit information
rightness.” In line with this proposition, medial prefrontal damage between these cortices is related to disorders of attentional and of
often spares the ability to retrieve AMs; however, these memories conscious processing (Carrera & Bogousslavsky, 2006; Crone et al., 2014;
are prone to monitoring impairments (Gilboa et al., 2006). Located in van Der Werf, Jolles, Witter, & Uylings, 2003). Notably, the cluster of
close proximity to the medial prefrontal cortices, the perigenual activation revealed by the meta‐analysis was specific to midline and
anterior cingulate has been linked to emotional conflict evaluation dorsal thalamic nuclei, which are associated most strongly with salient
and is suggested to serve a role in emotion regulation via appraisal‐ and emotional stimulus processing (LeDoux, Farb, & Romanski, 1991;
based, top‐down strategies (Meyer‐Lindenberg & Tost, 2012). Metzger et al., 2010; Seeley et al., 2007; for review see Metzger, van der
In turn, the results revealed by our meta‐analyses for controls Werf, & Walter, 2013). In PTSD, the thalamus is evidenced to display
may be interpreted as an intact monitoring process during trauma‐ reduced activation during script‐driven symptom provocation as well as
related AM. In PTSD, compromised memory search and retrieval during rest (Frewen, Pain, Dozois, & Lanius, 2006; Kim et al., 2007; Lanius
monitoring may suggest a tendency to be overwhelmed by the et al., 2001, 2003; Liberzon, Taylor, Fig, & Koeppe, 1996; Yan et al., 2013;
THOME ET AL. | 17
Zhu et al., 2017). Moreover, the thalamus is demonstrated to exhibit in a state‐dependent, emotionally charged form that exhibits strong
reduced resting‐state functional connectivity with the medial prefrontal perceptual priming to trauma‐related material (Arntz et al., 2005;
and the anterior cingulate cortices in PTSD (Lanius et al., 2005; Yin et al., Brewin, 2014; Michael et al., 2005; van der Kolk & Fisler, 1995). Hence,
2011). Other studies also report decreased thalamic functional con- trauma‐related AMs in PTSD are more likely to be re‐experienced
nectivity, specifically the pulvinar nuclei, with more posteromedial vividly, as opposed to retrieved in a controlled manner (Berntsen et al.,
cortices in PTSD as compared with controls (Terpou et al., 2018; Yin 2003; Brewin, 2014; Ehlers et al., 2004). Northoff and Bermpohl (2004)
et al., 2011). These aberrant characteristics may restrict, in part, the relay have proposed a system where anterior midline structures (i.e., medial
of information between medial prefrontal and posteromedial cortices prefrontal, anterior cingulate) of the AM network engage the
during AM processes in PTSD. In turn, impaired thalamic modulation may monitoring, evaluation, and representation of AMs, whereas posterior
produce a disconnect between the medial prefrontal (i.e., retrieval midline structures (i.e., precuneus, posterior cingulate) engage self‐
monitoring processes) and the posteromedial (i.e., reliving and visual referential and visual imagery aspects of AMs (Spreng & Grady, 2010;
imagery processes) cortices during trauma‐related AM that is required to Svoboda et al., 2006). As a result, increased activation of posterior
engage into a controlled reliving experience (i.e., mental time traveling parietal structures may promote greater vividness during recollection
involving the reestablishment of sensory and of emotional components of of the sensory and the emotional features of the AM (Berntsen et al.,
the AM, while simultaneously activating the knowledge that this 2003; Ehlers et al., 2004). Notably, the PTSD group also showed an
experience is related to the past). increase in activation of the dorsal anterior cingulate, a robust finding
as it was generated by both meta‐analyses. The dorsal anterior
cingulate is associated with negatively valenced emotion processing, in
4.3 | AM network: PTSD > Control
particular the regulation of visceral sensations (Lieberman & Eisenber-
The meta‐analyses revealed several brain regions exhibiting more ger, 2015; Rainville, 2002). In turn, increased activation of the dorsal
common activation in participants with PTSD as compared with anterior cingulate may contribute to the vivid retrieval (i.e., bodily
trauma‐ and nontrauma‐exposed control subjects. Namely, the sensations) of trauma‐related AMs in participants with PTSD. These
precuneus, the posterior cingulate, the middle cingulate, and the findings are also consistent with the centrality of trauma to personal
parahippocampal gyrus were reported to display greater activation identity in PTSD, where re‐experiencing of the trauma, as mediated by
in the PTSD group during trauma‐related AM recollection as posterior parietal activation (e.g., posterior cingulate, precuneus), may
compared with controls. These findings corroborate reports by integrate with an individual’s sense of self (Berntsen & Rubin, 2007;
Sartory et al. (2013), where the posterior parietal and the poster- Berntsen et al., 2003).
omedial cortices were activated more commonly in their PTSD In addition to the posterior parietal and the posteromedial
sample as well. Interestingly, the posterior parietal and the cortices, the parahippocampal gyrus also demonstrated more consis-
parahippocampal gyrus activation revealed across the recollection tent activation during trauma‐related AM recollection in the PTSD
analyses was also found in analyses specific to trauma‐related AM group as compared with controls. The parahippocampal gyrus is part
retrieval. Given that these regions are thought to underlie the self‐ of the limbic system and plays a role in memory encoding as well as
referential and the visual imagery aspects of AM (Spreng & Grady, emotional and anxiety‐related processing (Kilpatrick & Cahill, 2003;
2010; Svoboda et al., 2006), neural activation of these structures Nordahl et al., 1990; Reiman, Fusselman, Fox, & Raichle, 1989; Reiman,
during retrieval phases provides evidence for rapid re‐experiencing Raichle, Butler, Herscovitch, & Robins, 1984). During a resting‐state
of trauma‐related AMs following exposure to trauma‐related stimuli functional connectivity analysis conducted by Ward et al. (2014) with
in persons with PTSD (Ehlers et al., 2004). Moreover, the meta‐ healthy participants, the parahippocampal gyrus was shown to display
analyses on re‐experiencing processes revealed greater common the strongest connectivity of multiple medial temporal lobe regions
activation of the ventromedial prefrontal and the dorsal anterior with the DMN. The authors suggested that the parahippocampal gyrus
cingulate in the PTSD group as compared with controls. Although may be the primary hub mediating the relationship between the
these analyses are based on a small study sample (N = 6), they may medial temporal lobe and the DMN (Ward et al., 2014). Interestingly,
provide evidence for the delayed recruitment of memory search and the parahippocampal gyrus is shown to exhibit a decrease in functional
retrieval monitoring processes (i.e., medial prefrontal cortices) in connectivity with the central node of the DMN, the posterior
PTSD, a seemingly opposite trend to that of healthy control cingulate, in individuals with PTSD during rest (Bluhm et al., 2009).
subjects. In line with the present meta‐analysis, emerging evidence suggests
Autobiographical memories in PTSD are thought to be distinct in that the DMN may be recruited to a greater extent during trauma‐
form from AMs recollected in controls; however, it is important to note related processing in PTSD as compared with controls (Daniels,
that this interpretation does not refer to a specific feature of a study Frewen, McKinnon, & Lanius, 2011; Nicholson et al., 2018; Terpou
design. In participants with PTSD, some traumatic memories are said to et al., 2019). Here, Terpou et al. (2019) have suggested that
remain in an unprocessed state, where sensory, emotional, and participants with PTSD may experience greater self‐related proces-
cognitive components of the AM are fragmented, or are dissociated sing, as indicated by DMN recruitment, during trauma‐related stimulus
(Berntsen et al., 2003; McKinnon, Brewer, Cameron, & Nixon, 2017; St exposure as compared with during resting‐state. In closing, the
Jacques, Kragel, & Rubin, 2013). These AMs are proposed to be stored increased activation of the parahippocampal gyrus may reflect an
18 | THOME ET AL.
increased engagement of the DMN during trauma‐related AM systems, which are shown to be associated with greater PTSD
recollection in participants with PTSD. symptom severity.
4.5 | Limitations
4.4 | AM and implicit memory systems
There are several limitations to consider. The presented meta‐
Interestingly, the within‐group meta‐analysis of PTSD, but not analyses revealed altered common activation in high‐order cortical
the control group, revealed activation of the caudate nucleus, a regions during trauma‐related AM recollection in PTSD as compared
region more characteristic of implicit memory systems, during with controls, namely enhanced common activation of posteromedial
trauma‐related AM recollection. The caudate is part of the dorsal cortices, with concomitant reduced recruitment of medial prefrontal
striatum, which functions during procedural, associative, and emo- brain activation. Despite a more common activation of the
tional learning processes (McDonald & White, 1993; Packard, Cahill, parahippocampal gyrus in PTSD as compared with controls, the
& McGaugh, 1994; Setlow, 1997). Procedural memory is thought to present meta‐analyses did not reveal more common activation of the
be acquired after many repetitions of a certain behaviour, after amygdala, or deeper‐layer brain regions (e.g., periaqueductal gray)
which the behaviour transitions from an explicit to an implicit underlying affective processing in general, which has been discussed
representation (Kandel et al., 2012; Maddox & Ashby, 2004; Poldrack frequently as contributing to the emotional intensity during trauma‐
& Packard, 2003). The implicit representation of a procedural related AMs in PTSD (e.g., Brewin, 2018; Maddox et al., 2019).
memory relies on the ventral and the dorsal striatum, the substantia Generally, deep‐layer brain regions are smaller in size, which
nigra, the subthalamic nuclei as well as the precentral gyri of the increases the difficulty to demarcate these structures with meta‐
cortex (Henke, 2010; Kandel et al., 2012). Here, activation of the analytical techniques assuming a strong overlap. Second, many
caudate and the precentral gyri may be interpreted as an increase in studies included in the meta‐analyses investigated rather small data
procedural‐based memory storage of a patient’s trauma memory. sets (with some studies including only six subjects in one experi-
Given the intrusive and the vivid nature of trauma‐related AMs mental group; e.g., Driessen et al., 2004), which result in increased
(Berntsen et al., 2003; St Jacques et al., 2013), frequent re‐ between‐study variance, while at the same time, reducing statistical
experiencing of the trauma memory may promote a transition to power (Button et al., 2013). Third, it is important to mention that the
greater implicit storage of the procedural component. Although little identified studies did apply different experimental paradigms in
is known on the differences expressed by the procedural memory general (i.e., script‐driven imagery, trauma‐related stimulus presenta-
system in PTSD, it is well‐established that individuals with PTSD tion), as well as different stimulus modalities in particular (i.e., visual,
show a physiological hypersensitivity to threat stimuli (Blechert, auditory), which is likely to be related to different neural substrates.
Michael, & Wilhelm, 2019; Niles et al., 2018; Rabellino et al., 2017; However, given the number of identified studies, creating further
Seligowski et al., 2019; Young et al., 2018). In particular, trauma‐ subcategories would have resulted in subgroups that were too small
related stimuli generate an increased expression of the sympathetic to conduct meaningful analyses by virtue of the increased difficulty
nervous system, which is identified behaviourally by altered startle to observe common activation. Lastly, it is important to note that
responses in persons with PTSD (D’Andrea, Pole, DePierro, Freed, & PTSD has been recognized as a heterogenous disorder, ranging from
Wallace, 2013; Grillon & Morgan, 1999; McTeague et al., 2010; presentations with predominant states of hypervigilance to states of
Thome et al., 2018), as well as upregulated defensive responses (i.e. detachment (i.e., derealization, depersonalization), with the latter
fight, flight, freeze) in animal models of PTSD (Dean, 2011; being more often associated to the recently formulated dissociative
Hagenaars, Oitzl, & Roelofs, 2014; Vianna, Szapiro, McGaugh, subtype (Fenster et al., 2018; Lanius et al., 2018). In addition, PTSD is
Medina, & Izquierdo, 2001). The enhanced sympathetic reactivity often associated with several comorbidities, like, for example, major
may include a motor component, to be represented by the procedural depressive disorder or substance use disorders (Driessen, Schulte
memory system. These sympathetic‐mediated alterations may also et al., 2008; Nichter, Norman, Haller, & Pietrzak, 2019; Pietrzak,
relate to associative memory processes (LeDoux, 2003). In line with Goldstein, Southwick, & Grant, 2011). However, due to the limited
this proposition, both the caudate and a cluster encompassing the number of identified studies, creating sufficiently sized subgroups for
amygdala, the hippocampus, and the insula revealed common each of the possible combinations was not possible. Future work is
activation correlating positively with PTSD symptom severity in the needed urgently to disentangle potential confounding or moderating
PTSD group. The amygdala and the hippocampus are implicated in variables and their influence on trauma‐related AM recollection.
the learning and the memory of associative and of nonassociative
fear responses involved during trauma‐related AM processing
4.6 | Conclusion
(Golier, Yehuda, Lupien, & Harvey, 2003; Lambert & McLaughlin,
2019; Maddox, Hartmann, Ross, & Ressler, 2019; van der Kolk, 1994; These meta‐analyses investigate the differences in common activation
Werner et al., 2009). Taken together, activation of the caudate, the of the AM network during retrieval and re‐experiencing of trauma‐
amygdala, and the hippocampus during trauma‐related AM may related AMs in participants with PTSD as compared with controls. The
suggest a greater storage of trauma material toward implicit memory AM network is shown to demonstrate broadly group‐specific
THOME ET AL. | 19
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The Neural Correlates of Trauma Related Autobiographical Memory in Posttraumatic Stress Disorder: A Meta Analysis

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The Neural Correlates of Trauma Related Autobiographical Memory in Posttraumatic Stress Disorder: A Meta Analysis

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Received: 23 July 2019 | Revised: 2 October 2019 | Accepted: 6 November 2019

The neural correlates of trauma‐related autobiographical

Janine Thome1,2 | Braeden A. Terpou3 | Margaret C. McKinnon4,5,6 | Ruth A. Lanius1,3

Memory is the process by which information is extracted through

Depress Anxiety. 2019;1–25. wileyonlinelibrary.com/journal/da © 2019 Wiley Periodicals, Inc. | 1

T A B L E 1A fMRI studies on trauma‐related AM in PTSD: Sample and paradigm description

N = 5; note that none of the “reexperiencing” studies included a

Trauma script > negative

After stimpres/delay 30 s/duration Trauma script > neutral

After stimpres/delay 30 s/duration Trauma script > neutral

Trauma script > neutral

During stimulus presentation

negative correlations of PTSD symptom severity and common brain

general (i.e., dissociation, anxiety), as only a few studies were

2.2 | Experimental contrast selection

we were interested in both the voluntary retrieval and the

subsequent re‐experiencing of the trauma‐related AM as well as

studies employing trauma‐related material to evoke traumatic

trauma‐exposed controls. Hence, reported common brain activation

retrieval and re‐experiencing of a trauma memory, but rather also

Trauma‐related material included trauma‐related AM scripts as

well as trauma‐related stimuli (i.e., words, images, sounds), which

neutral or a negative stimulus, or to a baseline condition in a few

(N = 6) were included in the current analyses. Activation foci of the

and re‐experiencing), (b) studies categorized as specific to trauma‐

related AM retrieval, and (c) studies categorized as specific to

trauma‐related AM re‐experiencing; where each of the identified

studies was represented only once in each meta‐analysis to avoid

conducted on the differences between participants with PTSD as

control condition that was most alike to the experimental condition

T A B L E 1B fMRI studies on trauma‐related AM in PTSD: Analysis approach and contrast description

MNI coordinates Cluster

Contrast R/L Brain region x y z SDM‐Z p Size BA Jackknife

MNI coordinates Cluster

Contrast R/L Brain region x y z SDM‐Z p Size BA Jackknife

3.1.1 | Controls: Within‐group trauma‐related AM

Contrast R/L Brain region x y z SDM‐Z p Size BA Jackknife

3.3.4 | PTSD > Control: Between‐group comparison

3.3.1 | Controls: Within‐group trauma‐related AM

3.3.2 | PTSD: Within‐group trauma‐related AM 4.1 | Overview

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