Cited by 34Posttraumatic Stress Disorder ResearchMemory and Neural MechanismsSpatial Cognition and Navigation

Impaired allocentric spatial processing in posttraumatic stress disorder

Open access
Smith, Kirsten V., Burgess, Neil, Brewin, Chris R., King, John A.·2015·Neurobiology of Learning and Memory

Abstract

A neurobiological dual representation model of PTSD proposes that reduced hippocampus-dependent contextual processing contributes to intrusive imagery due to a loss of control over hippocampus-independent sensory and affective representations. We investigated whether PTSD sufferers show impaired allocentric spatial processing indicative of reduced hippocampal functioning. Trauma-exposed individuals with (N=29) and without (N=30) a diagnosis of PTSD completed two tests of spatial processing: a topographical recognition task comprising perceptual and memory components, and a test of memory for objects' locations within a virtual environment in which the test is from either the same viewpoint as presentation (solvable with egocentric memory) or a different viewpoint (requiring allocentric memory). Participants in the PTSD group performed significantly worse on allocentric spatial processing than trauma-exposed controls. Groups performed comparably on egocentric memory and non-spatial memory for lists of objects. Exposure to repeated incident trauma was also associated with significantly worse spatial processing in the PTSD group. Results show a selective impairment in allocentric spatial processing, implicating weak hippocampal functioning, as predicted by a neurobiological dual representation model of PTSD. These findings have important clinical implications for cognitive therapy.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.nlm.2015.01.007

Cites

6 of 6 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Exposure to previous trauma is associated with a greater impairment in specific aspects of spatial processing.

    “In this study and in a separate study of navigation [37], exposure to previous trauma was associated with a greater impairment in specific aspects of spatial processing.”

    From Memory and Forgetting (2018) · cites this paper as [36]

  • PTSD patients appear to have a selective deficit in allocentric spatial memory, implicating weaker hippocampal functioning.

    “Consistent with this model, PTSD patients appear to have a selective deficit in allocentric spatial memory, implicating weaker hippocampal functioning [36].”

    From Memory and Forgetting (2018) · cites this paper as [36]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 40

  1. Abrahams S. Morris R.G. Polkey C.E. Jarosz J.M. Cox T.C. Graves M. Hippocampal involvement in spatial and working memory: A structural MRI analysis of patients with unilateral medial temporal lobe sclerosis Brain and Cognition 41 1999 39 65 10536085
  2. Astur R.S. German S.A. St Tolin D. Ford J. Russell D. Stevens M. Hippocampus function predicts severity of post-traumatic stress disorder Cyberpsychology & Behavior 9 2006 234 240 16640486
  3. Bisby J. King J.A. Brewin C.R. Burgess N. Curran H.V. Acute effects of alcohol on intrusive memory development and viewpoint dependence in spatial memory support a dual representation model Biological Psychiatry 68 2010 280 286 20202625
  4. Bonne O. Brandes D. Gilboa A. Gomori J.M. Shenton M.E. Pitman R.K. Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD American Journal of Psychiatry 158 2001 1248 1254 11481158 PMC2819102
  5. Bremner J. Hypotheses and controversies related to effects of stress on the hippocampus: An argument for stress-induced damage to the hippocampus in patients with posttraumatic stress disorder 2001 John Wiley & Sons Inc. 11345127
  6. Bremner J.D. Vythilingam M. Vermetten E. Southwick S.M. McGlashan T. Nazeer A. MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder American Journal of Psychiatry 160 2003 924 932 12727697
  7. Brewin C.R. Posttraumatic stress disorder: Malady or myth? 2003 Yale University Press New Haven, Connecticut
  8. Brewin C.R. Gregory J.D. Lipton M. Burgess N. Intrusive images in psychological disorders: Characteristics, neural mechanisms, and treatment implications Psychological Review 117 2010 210 232 20063969 PMC2834572
  9. Burgess N. Spatial memory: How egocentric and allocentric combine Trends in Cognitive Sciences 10 2006 551 557 17071127
  10. Burgess N. Maguire E.A. O’Keefe J. The human hippocampus and spatial and episodic memory Neuron 35 2002 625 641 12194864
  11. Byrne P. Becker S. Burgess N. Remembering the past and imagining the future: A neural model of spatial memory and imagery Psychological Review 114 2007 340 375 17500630 PMC2678675
  12. Carrion V.G. Weems C.F. Eliez S. Patwardhan A. Brown W. Ray R.D. Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder Biological Psychiatry 50 2001 943 951 11750890
  13. Cohen N. Eichenbaum H. Memory, amnesia, and the hippocampal system 1993 The MIT Press Cambridge, MA
  14. De Bellis M.D. Keshavan M.S. Shifflett H. Iyengar S. Beers S.R. Hall J. Brain structures in pediatric maltreatment-related posttraumatic stress disorder: A sociodemographically matched study Biological Psychiatry 52 2002 1066 1078 12460690
  15. Ehlers A. Clark D.M. A cognitive model of posttraumatic stress disorder Behaviour Research and Therapy 38 2000 319 345 10761279
  16. Eichenbaum H. Cohen N.J. Representation in the hippocampus – What do hippocampal neurons code? Trends in Neurosciences 11 1988 244 248 2465617
  17. Farah M.J. Hammond K.M. Mental rotation and orientation-invariant object recognition: Dissociable processes Cognition 29 1988 29 46 3402190
  18. Geuze E. Vermetten E. Ruf M. de Kloet C.S. Westenberg H.G. Neural correlates of associative learning and memory in veterans with posttraumatic stress disorder Journal of Psychiatric Research 42 2008 659 669 17698081
  19. Gilbertson M.W. Shenton M.E. Ciszewski A. Kasai K. Lasko N.B. Orr S.P. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma Nature Neuroscience 5 2002 1242 1247 PMC2819093 12379862
  20. Gilbertson M.W. Williston S.K. Paulus L.A. Lasko N.B. Gurvits T.V. Shenton M.E. Configural cue performance in identical twins discordant for posttraumatic stress disorder: Theoretical implications for the role of hippocampal function Biological Psychiatry 62 2007 513 520 17509537 PMC2768050
  21. Golier J.A. Yehuda R. Lupien S.J. Harvey P.D. Grossman R. Elkin A. Memory performance in Holocaust survivors with posttraumatic stress disorder American Journal of Psychiatry 159 2002 1682 1688 12359673
  22. Gomez A. Cerles M. Rousset S. Rémy C. Baciu M. Differential hippocampal and retrosplenial involvement in egocentric-updating, rotation, and allocentric processing during online spatial encoding: An fMRI study Frontiers in Human Neuroscience 8 2014 1 14 24688464 PMC3960510
  23. Guez J. Naveh-Benjamin M. Yankovsky Y. Cohen J. Shiber A. Shalev H. Traumatic stress is linked to a deficit in associative episodic memory Journal of Traumatic Stress 24 2011 260 267 21523830
  24. Gurvits T.V. Shenton M.E. Hokama H. Ohta H. Lasko N.B. Gilbertson M.W. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder Biological Psychiatry 40 1996 1091 1099 8931911 PMC2910907
  25. Hartley T. Bird C.M. Chan D. Cipolotti L. Husain M. Vargha-Khadem F. The hippocampus is required for short-term topographical memory in humans Hippocampus 17 2007 34 48 17143905 PMC2677717
  26. Holdstock J.S. Mayes A.R. Cezayirli E. Isaac C.L. Aggleton J.P. Roberts N. A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage Neuropsychologia 38 2000 410 425 10683392
  27. Hupbach A. Gomez R. Hardt O. Nadel L. Reconsolidation of episodic memories: A subtle reminder triggers integration of new information Learning and Memory 14 2007 47 53 17202429 PMC1838545
  28. Karl A. Schaefer M. Malta L.S. Dörfel D. Rohleder N. Werner A. A meta-analysis of structural brain abnormalities in PTSD Neuroscience and Biobehavioral Reviews 30 2006 1004 1031 16730374
  29. King J.A. Burgess N. Hartley T. Vargha-Khadem F. O’Keefe J. Human hippocampus and viewpoint dependence in spatial memory Hippocampus 12 2002 811 820 12542232
  30. King J.A. Trinkler I. Hartley T. Vargha-Khadem F. Burgess N. The hippocampal role in spatial memory and the familiarity-recollection distinction: A case study Neuropsychology 18 2004 405 417 15291719
  31. Lee A.C. Buckley M.J. Pegman S.J. Spiers H. Scahill V.L. Gaffan D. Specialization in the medial temporal lobe for processing of objects and scenes Hippocampus 15 2005 782 797 16010661
  32. O’Keefe J. Nadel L. The hippocampus as a cognitive map 1978 Clarendon Press Oxford
  33. Perez C.M. Widom C.S. Childhood victimization and long-term intellectual and academic outcomes Child Abuse and Neglect 18 1994 617 633 7953902
  34. Pitman R.K. Rasmusson A.M. Koenen K.C. Shin L.M. Orr S.P. Gilbertson M.W. Biological studies of post-traumatic stress disorder Nature Reviews Neuroscience 13 2012 769 787 PMC4951157 23047775
  35. Scoville W.B. Milner B. Loss of recent memory after bilateral hippocampal lesions Journal of Neurology, Neurosurgery and Psychiatry 20 1957 11 21 PMC497229 13406589
  36. Seidler G.H. Wagner F.E. Comparing the efficacy of EMDR and trauma-focused cognitive-behavioral therapy in the treatment of PTSD: A meta-analytic study Psychological Medicine 36 2006 1515 1522 16740177
  37. Spiers H. Burgess N. Hartley T. Vargha-Khadem F. O’Keefe J. Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching Hippocampus 11 2001 715 725 11811666
  38. Squire L.R. Zola-Morgan S. The medial temporal lobe memory system Science 253 1991 1380 1386 1896849
  39. Tempesta D. Mazza M. Iaria G. De Gennaro L. Ferrara M. A specific deficit in spatial memory acquisition in post-traumatic stress disorder and the role of sleep in its consolidation Hippocampus 22 2012 1154 1163 21739522
  40. Yehuda R. Golier J.A. Tischler L. Harvey P.D. Newmark R. Yang R.K. Hippocampal volume in aging combat veterans with and without post-traumatic stress disorder: Relation to risk and resilience factors Journal of Psychiatric Research 41 2007 435 445 16445942

Cited by

Sorted by citations

Authors
Smith, K. V., Burgess, N., Brewin, C. R., & King, J. A.
Affiliations
  • Royal Holloway University of London (GB)
  • UCL Queen Square Institute of Neurology (GB)
  • University College London (GB)
Corresponding author
Smith, Kirsten V.
Venue
Neurobiology of Learning and Memory
Publisher
Elsevier BV
Published
2015-03
Volume
119
Pages
69-76
ISSN
1074-7427 (ISSN-L)
OpenAlex
W2103902807
Cited by
34
References
6
Citations by year
2026: 2 · 2025: 3 · 2024: 3 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 4 · 2018: 2 · 2017: 6 · 2016: 2 · 2015: 1
FWCI
4.55
Type
journal article
Language
en
Open access
Locations
  • Neurobiology of Learning and Memory (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
  • Psychological Therapies Service
  • CADAT
Topics
  • Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
Keywords
post-traumatic stress disorder, hippocampus, virtual navigation, intrusive imagery, spatial memory impairment
MeSH terms
Adolescent, Adult, Aged, Female, Hippocampus, Humans, Male, Middle Aged, Space Perception, Stress Disorders, Post-Traumatic, Recognition, Psychology, Young Adult, Spatial Memory

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