Episodic memory after trauma exposure: Medial temporal lobe function is positively related to re-experiencing and inversely related to negative affect symptoms
Open accessAbstract
Hippocampal structure is particularly sensitive to trauma and other stressors. However, previous findings linking hippocampal function with trauma-related psychopathology have been mixed. Heterogeneity in psychological responses to trauma has not been considered with respect to hippocampal function and may contribute to mixed findings. To address these issues, we examined associations between data-driven symptom dimensions and episodic memory formation, a key function of the hippocampus, in a trauma-exposed sample. Symptom dimensions were defined using principal components analysis (PCA) in 3881 trauma-exposed African-American women recruited from primary care waiting rooms of a large urban hospital. Hippocampal and amygdala function were subsequently investigated in an fMRI study of episodic memory formation in a subset of 54 women. Participants viewed scenes with neutral, negative, and positive content during fMRI, and completed a delayed cued recall task. PCA analysis produced five symptom dimensions interpreted as reflecting negative affect, somatic symptoms, re-experiencing, hyper-arousal, and numbing. Re-experiencing was the only symptom type associated with hippocampal function, predicting increased memory encoding-related activation in the hippocampus as well as the amygdala. In contrast, the negative affect component predicted lower amygdala activation for subsequently recalled scenes, and lower functional coupling with other important memory-related regions including the precuneus, inferior frontal gyrus, and occipital cortex. Symptom dimensions were not related to hippocampal volume. The fMRI findings for re-experiencing versus negative affect parallel differences in behavioral memory phenomena in PTSD versus MDD, and highlight a need for more complex models of trauma-related pathology.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Re-experiencing was the only symptom type associated with amygdala function, predicting increased amygdala activation.
“Re-experiencing was the only symptom type associated with amygdala function, predicting increased amygdala activation.”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Stevens et al. (2018)
The Results section on memory encoding-related fMRI activation reports that re-experiencing was positively associated with amygdala activation. But it also reports an inverse association for negative affect, so re-experiencing was not the only symptom type associated with amygdala activation. (LLM, conf=0.90)
Experimental — accuracy not yet measuredStevens et al. (2018) PCA on 3881 trauma-exposed African American women elicited five symptom dimensions interpreted as negative affect, somatic symptoms, re-experiencing, hyperarousal, and numbing.
“PCA analysis elicited five symptom dimensions interpreted as reflecting negative effect, somatic symptoms, re-experiencing, hyperarousal, and numbing.”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Stevens et al. (2018)
The negative affect component predicted lower amygdala activation for subsequently recalled scenes.
“In contrast, the negative affect component predicted lower amygdala activation for subsequently recalled scenes (Stevens et al., 2018).”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Stevens et al., 2018
Symptom dimensions were not associated with hippocampal volume.
“Symptom dimensions were not associated with hippocampal volume.”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Stevens et al. (2018)
Reliving was the only symptom related to hippocampal function, predicting increased activation associated with memory encoding in the hippocampus and amygdala.
“Reliving was the only symptom related to hippocampal function, predicting an increased activation associated with memory encoding in the hippocampus and amygdala.”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Stevens et al. (2018)
Stevens et al. (2018) found that hippocampal activation is increased in relation to symptoms of reliving.
“Stevens et al. (2018) investigated a relationship between hippocampal activation and symptoms of reliving, and came to the result that such activation is increased.”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Stevens et al. (2018)
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
The citation lists haven’t been fetched yet
References 57 · Cited by 49
Research works printed but not linked: 39
- Ai H. Opmeer E.M. Veltman D.J. van der Wee N.J. van Buchem M.A. Aleman A. van Tol M.-J. Brain activation during emotional memory processing associated with subsequent course of depression Neuropsychopharmacology 40 10 2015 2454 2463 25857684 PMC4538361
- Amunts K. Kedo O. Kindler M. Pieperhoff P. Mohlberg H. Shah N.J. … Zilles K. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps Anat. Embryol. 210 5 2005 343 352 16208455
- Bearden C.E. Glahn D.C. Monkul E.S. Barrett J. Najt P. Villarreal V. Soares J.C. Patterns of memory impairment in bipolar disorder and unipolar major depression Psychiatry Res. 142 2–3 2006 139 150 16631256
- Breslau N. Davis G.C. Peterson E.L. Schultz L.R. A second look at comorbidity in victims of trauma: the posttraumatic stress disorder-major depression connection Biol. Psychiatry 48 9 2000 902 909 11074228
- Brittlebank A. Scott J. Williams J.M. Ferrier I. Autobiographical memory in depression: state or trait marker? Br. J. Psychiatry 162 1 1993 118 121 8425125
- Brohawn K.H. Offringa R. Pfaff D.L. Hughes K.C. Shin L.M. The neural correlates of emotional memory in posttraumatic stress disorder Biol. Psychiatry 68 11 2010 1023 1030 20855060
- Burt D.B. Zembar M.J. Niederehe G. Depression and memory impairment: a meta-analysis of the association, its pattern, and specificity Psychol. Bull. 117 2 1995 285 305 7724692
- Cahill L. McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory Trends Neurosci. 21 7 1998 294 299 9683321
- Dickie E.W. Brunet A. Akerib V. Armony J.L. An fMRI investigation of memory encoding in PTSD: influence of symptom severity Neuropsychologia 46 5 2008 1522 1531 18321537
- Dickie E.W. Brunet A. Akerib V. Armony J.L. Neural correlates of recovery from post-traumatic stress disorder: a longitudinal fMRI investigation of memory encoding Neuropsychologia 49 7 2011 1771 1778 21382385
- Eichenbaum H. Hippocampus: cognitive processes and neural representations that underlie declarative memory Neuron 44 1 2004 109 120 15450164
- Foa E.B. Tolin D.F. Comparison of the PTSD symptom scale-interview version and the clinician-administered PTSD scale J. Trauma. Stress. 13 2 2000 181 191 10838669
- Garfinkel S.N. Abelson J.L. King A.P. Sripada R.K. Wang X. Gaines L.M. Liberzon I. Impaired contextual modulation of memories in PTSD: an fMRI and psychophysiological study of extinction retention and fear renewal J. Neurosci. 34 40 2014 13435 13443 25274821 PMC4262698
- Gillespie C.F. Bradley B. Mercer K. Smith A.K. Conneely K. Gapen M. … Ressler K.J. Trauma exposure and stress-related disorders in inner city primary care patients Gen. Hosp. Psychiatry 31 6 2009 505 514 19892208 PMC2785858
- Gottesman I.I. Gould T.D. The endophenotype concept in psychiatry: etymology and strategic intentions Am. J. Psychiatr. 160 4 2003 636 645 12668349
- Hamann S. Ely T.D. Grafton S.T. Kilts C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli Nat. Neurosci. 2 3 1999 289 10195224
- Hayes J.P. LaBar K.S. McCarthy G. Selgrade E. Nasser J. Dolcos F. Morey R.A. Reduced hippocampal and amygdala activity predicts memory distortions for trauma reminders in combat-related PTSD J. Psychiatr. Res. 45 5 2011 660 669 21047644 PMC3081889
- Jovanovic T. Norrholm S.D. Blanding N.Q. Davis M. Duncan E. Bradley B. Ressler K.J. Impaired fear inhibition is a biomarker of PTSD but not depression Depress. Anxiety 27 3 2010 244 251 20143428 PMC2841213
- Kaczkurkin A.N. Burton P.C. Chazin S.M. Manbeck A.B. Espensen-Sturges T. Cooper S.E. Sponheim S.R. Lissek S. Neural substrates of overgeneralized conditioned fear in PTSD Am. J. Psychiatry 174 2 2017 125 134 27794690 PMC7269602
- Kessler R.C. Berglund P. Demler O. Jin R. Merikangas K.R. Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication Arch. Gen. Psychiatry 62 6 2005 593 602 15939837
- Levine L.J. Edelstein R.S. Emotion and memory narrowing: a review and goal-relevance approach Cognit. Emot. 23 5 2009 833 875
- Lindauer R.J.L. Vlieger E.-J. Jalink M. Olff M. Carlier I.V.E. Majoie C.B.L.M. … Gersons B.P.R. Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder Biol. Psychiatry 56 5 2004 356 363 15336518
- Logue M.W. van Rooij S.J Dennis E.L. Davis S.L. Hayes J.P. Stevens J.S. … Koch S.B. Smaller hippocampal volume in posttraumatic stress disorder: a multi-site ENIGMA-PGC study Biol. Psychiatry 2017 E-pub ahead of print PMC5951719 29217296
- Mather M. Sutherland M.R. Arousal-biased competition in perception and memory Perspect. Psychol. Sci. 6 2 2011 114 133 21660127 PMC3110019
- McGaugh J.L. Memory consolidation and the amygdala: a systems perspective Trends Neurosci. 25 9 2002 456 461 12183206
- Miller D.R. Hayes S.M. Hayes J.P. Spielberg J.M. Lafleche G. Verfaellie M. Default mode network subsystems are differentially disrupted in posttraumatic stress disorder Biol. Psychiatry 2 4 2017 363 371 Cognitive Neuroscience and Neuroimaging PMC5396184 28435932
- Murty V.P. Ritchey M. Adcock R.A. LaBar K.S. fMRI studies of successful emotional memory encoding: a quantitative meta-analysis Neuropsychologia 48 12 2010 3459 3469 20688087 PMC2949536
- Riem M.M. Alink L.R. Out D. Van Ijzendoorn M.H. Bakermans-Kranenburg M.J. Beating the brain about abuse: empirical and meta-analytic studies of the association between maltreatment and hippocampal volume across childhood and adolescence Dev. Psychopathol. 27 02 2015 507 520 25997768
- Satterthwaite T.D. Cook P.A. Bruce S.E. Conway C. Mikkelsen E. Satchell E. … Sheline Y.I. Dimensional depression severity in women with major depression and post-traumatic stress disorder correlates with fronto-amygdalar hypoconnectivty Mol. Psychiatry 21 7 2016 894 902 26416545 PMC4840084
- Shalev A.Y. Freedman S. Peri T. Brandes D. Sahar T. Orr S.P. Pitman R.K. Prospective study of posttraumatic stress disorder and depression following trauma Am. J. Psychiatry 155 5 1998 630 637 9585714
- Simms L.J. Watson D. Doebbelling B.N. Confirmatory factor analyses of posttraumatic stress symptoms in deployed and nondeployed veterans of the Gulf war J. Abnorm. Psychol. 111 4 2002 637 12428777
- Squire L.R. Zola-Morgan S. The medial temporal lobe memory system Science 253 5026 1991 1380 1386 1896849
- Thomaes K. Dorrepaal E. Draijer N.P.J. de Ruiter M.B. Elzinga B.M. van Balkom A.J. … Veltman D.J. Increased activation of the left hippocampus region in complex PTSD during encoding and recognition of emotional words: a pilot study Psychiatry Res. Neuroimaging 171 1 2009 44 53 19081708
- Thomaes K. Dorrepaal E. Draijer N. de Ruiter M.B. Elzinga B.M. Sjoerds Z. … Veltman D.J. Increased anterior cingulate cortex and hippocampus activation in complex PTSD during encoding of negative words Soc. Cogn. Affect. Neurosci. 8 2 2013 190 200 22156722 PMC3575721
- van Tol M.-J. Demenescu L.R. van der Wee N.J.A. Kortekaas R. Marjan M.A.N. Boer J.A.D. … Veltman D.J. Functional magnetic resonance imaging correlates of emotional word encoding and recognition in depression and anxiety disorders Biol. Psychiatry 71 7 2012 593 602 22206877
- Tulving E. Episodic memory: from mind to brain Annu. Rev. Psychol. 53 1 2002 1 25 11752477
- Tulving E. Markowitsch H.J. Episodic and declarative memory: role of the hippocampus Hippocampus 8 3 1998 198 204 9662134
- Whisman M.A. Perez J.E. Ramel W. Factor structure of the Beck depression inventory—second edition(BDI-ii) in a student sample J. Clin. Psychol. 56 4 2000 545 551 10775046
- Williams J. Scott J. Autobiographical memory in depression Psychol. Med. 18 3 1988 689 695 3186869
- Authors
- Stevens, J. S., Reddy, R., Kim, Y. J., van Rooij, S. J. H., Ely, T. D., Hamann, S., Ressler, K. J., & Jovanovic, T.
- Affiliations
- Emory University (US)
- Harvard University (US)
- Corresponding author
- Stevens, Jennifer S.
- Venue
- NeuroImage: Clinical
- Publisher
- Elsevier BV
- Published
- 2018
- Volume
- 17
- Pages
- 650-658
- ISSN
- 2213-1582 (ISSN-L)
- PMC
- PMC5709292
- OpenAlex
- W2770072520
- Cited by
- 49
- References
- 57
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 6 · 2023: 8 · 2022: 11 · 2021: 2 · 2020: 4 · 2019: 2 · 2018: 4
- FWCI
- 3.39
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- NeuroImage Clinical (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Institutes of Mental Health (F32 MH101976, MH071537, MH098212)
- Emory and Grady Memorial Hospital General Clinical Research Center (UL1TR002378)
- NIH National Centers for Research Resources (M01RR00039)
- NIH (UL1TR000454)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- episodic memory, trauma exposure, hippocampus, amygdala, re-experiencing, negative affect, post-traumatic stress disorder, major depressive disorder, symptom dimensions, memory encoding, functional coupling, African American women, hippocampal volume
- MeSH terms
- Adult, Depression, Female, Humans, Image Interpretation, Computer-Assisted, Magnetic Resonance Imaging, Stress Disorders, Post-Traumatic, Temporal Lobe, Young Adult, Memory, Episodic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review