Cited by 49Posttraumatic Stress Disorder ResearchMemory Processes and InfluencesMemory and Neural Mechanisms

Episodic memory after trauma exposure: Medial temporal lobe function is positively related to re-experiencing and inversely related to negative affect symptoms

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Stevens, Jennifer S., Reddy, Renuka, Kim, Ye Ji, van Rooij, Sanne J.H., Ely, Timothy D., Hamann, Stephan, Ressler, Kerry J., Jovanovic, Tanja·2018·NeuroImage: Clinical

Abstract

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.

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References 57 · Cited by 49

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  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. Cahill L. McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory Trends Neurosci. 21 7 1998 294 299 9683321
  9. 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
  10. 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
  11. Eichenbaum H. Hippocampus: cognitive processes and neural representations that underlie declarative memory Neuron 44 1 2004 109 120 15450164
  12. 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
  13. 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
  14. 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
  15. Gottesman I.I. Gould T.D. The endophenotype concept in psychiatry: etymology and strategic intentions Am. J. Psychiatr. 160 4 2003 636 645 12668349
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. Levine L.J. Edelstein R.S. Emotion and memory narrowing: a review and goal-relevance approach Cognit. Emot. 23 5 2009 833 875
  22. 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
  23. 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
  24. Mather M. Sutherland M.R. Arousal-biased competition in perception and memory Perspect. Psychol. Sci. 6 2 2011 114 133 21660127 PMC3110019
  25. McGaugh J.L. Memory consolidation and the amygdala: a systems perspective Trends Neurosci. 25 9 2002 456 461 12183206
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. Squire L.R. Zola-Morgan S. The medial temporal lobe memory system Science 253 5026 1991 1380 1386 1896849
  33. 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
  34. 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
  35. 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
  36. Tulving E. Episodic memory: from mind to brain Annu. Rev. Psychol. 53 1 2002 1 25 11752477
  37. Tulving E. Markowitsch H.J. Episodic and declarative memory: role of the hippocampus Hippocampus 8 3 1998 198 204 9662134
  38. 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
  39. 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)
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
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

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