INTRODUCTION: Morphological correlates of nonpathological déjà vu (DV) have been identified recently within the human brain. Significantly reduced gray matter volume (GMV) within a set of cortical and subcortical regions reported in subjects experiencing DV seems to mirror the distribution of GMV reduction in mesial temporal lobe epilepsy (MTLE) patients but vary in terms of the hippocampus. Another condition associated with hippocampal GMV reduction and DV alike disturbance in memory processing is schizophrenia (SCH). Here, we tested the hypothesis that hippocampal involvement in nonpathological DV resembles more closely the pattern of GMV decrease observed in MTLE compared with that occurring in SCH. METHODS: Using automated segmentation of the MRI data we compared the medians of GMV within 12 specific hippocampal subfields in healthy individuals that do (DV+; N = 87) and do not report déjà vu experience (DV-; N = 26), and patients with MTLE (N = 47) and SCH (N = 29). By Pearson correlation, we then evaluated the similarity of MTLE and SCH groups to DV+ group with respect to spatial distribution of GMV deviation from DV- group. RESULTS: Significant GMV decrease was found in MTLE group in most of the subfields. There were just trends in the hippocampal GMV decrease found in DV+ or SCH groups. Concerning the spatial distribution of GMV decrease, we revealed statistically significant correlation for the left hippocampus for SCH vs DV+. Otherwise there was no statistically significant correlation. CONCLUSIONS: Our findings reveal structural features of hippocampal involvement in nonpathological DV, MTLE, and SCH. Despite our expectations, the pattern of GMV reduction in the DV+ relative to the DV- group does not resemble the pattern observed in MTLE any more than that observed in SCH. The highly similar patterns of the three clinical groups rather suggest an increased vulnerability of certain hippocampal subfields; namely, Cornu Ammonis (CA)4, CA3, dentate gyrus granular cell layer (GC-DG), hippocampal-amygdaloid transition area (HATA) and subiculum.

Behavioral and Social Neuroscience Research Group CEITEC Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Neurology Brno Epilepsy Center St Anne's University Hospital and Medical Faculty of Masaryk University Brno Czech Republic

Department of Psychiatry Faculty Hospital Brno and Medical Faculty of Masaryk University Brno Czech Republic

Multi modal and Functional Neuroimaging Research Group CEITEC Central European Institute of Technology Masaryk University Brno Czech Republic

Erratum In

Brain Behav. 2019 May;9(5):e01299. doi: 10.1002/brb3.1299. PubMed

See more in PubMed

Adachi, N. , Adachi, T. , Kimura, M. , Akanuma, N. , Takekawa, Y. , & Kato, M. (2003). Demographic and psychological features of déjà vu experiences in a nonclinical Japanese population. The Journal of Nervous and Mental Disease, 191, 242–247. 10.1097/01.NMD.0000061149.26296.DC PubMed DOI

Andersen, P. , Morris, R. , Amaral, D. , Bliss, T. , & OKeefe, J . (2006). The hippocampus book. London, UK: Oxford University Press; 10.1093/acprof:oso/9780195100273.001.0001 DOI

Bancaud, J. , Brunet‐Bourgin, F. , Chauvel, P. , & Halgren, E. (1994). Anatomical origin of déjà vu and vivid “memories” in human temporal lobe epilepsy. Brain: A Journal of Neurology, 117(Pt 1), 71–90. 10.1093/brain/117.1.71 PubMed DOI

Brambilla, P. , Perlini, C. , Rajagopalan, P. , Saharan, P. , Rambaldelli, G. , Bellani, M. , … Thompson, P. M. (2013). Schizophrenia severity, social functioning and hippocampal neuroanatomy: Three‐dimensional mapping study. The British Journal of Psychiatry: The Journal of Mental Science, 202, 50–55. 10.1192/bjp.bp.111.105700 PubMed DOI PMC

Brázdil, M. , Marecek, R. , Fojtíková, D. , Mikl, M. , Kuba, R. , Krupa, P. , & Rektor, I. (2009). Correlation study of optimized voxel‐based morphometry and (1)H MRS in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. Human Brain Mapping, 30, 1226–1235. 10.1002/hbm.20589 PubMed DOI PMC

Brázdil, M. , Mareček, R. , Urbánek, T. , Kašpárek, T. , Mikl, M. , Rektor, I. , & Zeman, A. (2012). Unveiling the mystery of déjà vu: The structural anatomy of déjà vu. Cortex, 48, 1240–1243. 10.1016/j.cortex.2012.03.004 PubMed DOI

Brázdil, M. , & Zeman, A. (2013). The boundaries of epilepsy: Where is the limit? A reply to Labate and Gambardella. Cortex, 49, 1163–1164. 10.1016/j.cortex.2012.09.015 PubMed DOI

Brown, A. S. (2003). A review of the déjà vu experience. Psychological Bulletin, 129, 394–413. 10.1037/0033-2909.129.3.394 PubMed DOI

Butterworth, P. , Cherbuin, N. , Sachdev, P. , & Anstey, K. J. (2012). The association between financial hardship and amygdala and hippocampal volumes: Results from the PATH through life project. Social Cognitive and Affective Neuroscience, 7, 548–556. 10.1093/scan/nsr027 PubMed DOI PMC

Byeon, J. H. , Kim, G.‐H. , Kim, J. Y. , Sun, W. , Kim, H. , & Eun, B.‐L. (2015). Cognitive dysfunction and hippocampal damage induced by hypoxic‐ischemic brain injury and prolonged febrile convulsions in immature rats. Journal of Korean Neurosurgical Society, 58, 22–29. 10.3340/jkns.2015.58.1.22 PubMed DOI PMC

Cascino, G. D. , Jack, C. R. , Parisi, J. E. , Sharbrough, F. W. , Hirschorn, K. A. , Meyer, F. B. , … O’Brien, P. C. (1991). Magnetic resonance imaging‐based volume studies in temporal lobe epilepsy: Pathological correlations. Annals of Neurology, 30, 31–36. 10.1002/ana.410300107 PubMed DOI

Cavazos, J. E. , Das, I. , & Sutula, T. P. (1994). Neuronal loss induced in limbic pathways by kindling: Evidence for induction of hippocampal sclerosis by repeated brief seizures. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 14, 3106–3121. 10.1523/JNEUROSCI.14-05-03106.1994 PubMed DOI PMC

Commission on Classification and Terminology of the International League Against Epilepsy . (1989). Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia, 30, 389–399. PubMed

Harrison, P. (2004). The hippocampus in schizophrenia: A review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berl.), 174, 151–162. 10.1007/s00213-003-1761-y PubMed DOI

Haukvik, U. K. , Westlye, L. T. , Mørch‐Johnsen, L. , Jørgensen, K. N. , Lange, E. H. , Dale, A. M. , … Agartz, I. (2015). In Vivo hippocampal subfield volumes in schizophrenia and bipolar disorder. Biological Psychiatry, 77, 581–588. 10.1016/j.biopsych.2014.06.020 PubMed DOI

Heckers, S. , Rauch, S. L. , Goff, D. , Savage, C. R. , Schacter, D. L. , Fischman, A. J. , & Alpert, N. M. (1998). Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature Neuroscience, 1, 318–323. 10.1038/1137 PubMed DOI

Hogan, R. E. (2001). Mesial temporal sclerosis: Clinicopathological correlations. Archives of Neurology, 58, 1484–1486. 10.1001/archneur.58.9.1484 PubMed DOI

Honea, R. , Crow, T. J. , Passingham, D. , & Mackay, C. E. (2005). Regional deficits in brain volume in schizophrenia: A meta‐analysis of voxel‐based morphometry studies. American Journal of Psychiatry, 162, 2233–2245. 10.1176/appi.ajp.162.12.2233 PubMed DOI

Iglesias, J. E. , Augustinack, J. C. , Nguyen, K. , Player, C. M. , Player, A. , Wright, M. , Roy, N. , Frosch, M. P. , … Alzheimer’s Disease Neuroimaging Initiative . (2015). A computational atlas of the hippocampal formation using ex vivo, ultra‐high resolution MRI: Application to adaptive segmentation of in vivo MRI. NeuroImage, 115, 117–137. 10.1016/j.neuroimage.2015.04.042 PubMed DOI PMC

Illman, N. A. , Butler, C. R. , Souchay, C. , & Moulin, C. J. A. (2012). Déjà experiences in temporal lobe epilepsy. Epilepsy Research and Treatment, 2012, 1–15. 10.1155/2012/539567 PubMed DOI PMC

Kapur, S. (2003). Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. American Journal of Psychiatry, 160, 13–23. 10.1176/appi.ajp.160.1.13 PubMed DOI

Kay, S. R. , Fiszbein, A. , & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13, 261–276. 10.1093/schbul/13.2.261 PubMed DOI

Keller, S. S. , & Roberts, N. (2008). Voxel‐based morphometry of temporal lobe epilepsy: An introduction and review of the literature. Epilepsia, 49, 741–757. 10.1111/j.1528-1167.2007.01485.x PubMed DOI

Kim, H. , Mansi, T. , Bernasconi, N. , & Bernasconi, A. (2012). Surface‐based multi‐template automated hippocampal segmentation: Application to temporal lobe epilepsy. Medical Image Analysis, 16, 1445–1455. 10.1016/j.media.2012.04.008 PubMed DOI

Kim, J. B. , Suh, S.‐I. , & Kim, J. H. (2015). Volumetric and shape analysis of hippocampal subfields in unilateral mesial temporal lobe epilepsy with hippocampal atrophy. Epilepsy Research, 117, 74–81. 10.1016/j.eplepsyres.2015.09.004 PubMed DOI

Kotloski, R. , Lynch, M. , Lauersdorf, S. , & Sutula, T. (2002). Repeated brief seizures induce progressive hippocampal neuron loss and memory deficits. Progress in Brain Research, 135, 95–110. 10.1016/S0079-6123(02)35010-6 PubMed DOI

Kühn, S. , Musso, F. , Mobascher, A. , Warbrick, T. , Winterer, G. , & Gallinat, J. (2012). Hippocampal subfields predict positive symptoms in schizophrenia: First evidence from brain morphometry. Translational Psychiatry, 2, e127 10.1038/tp.2012.51 PubMed DOI PMC

Labate, A. , Cerasa, A. , Mumoli, L. , Ferlazzo, E. , Aguglia, U. , Quattrone, A. , & Gambardella, A. (2015). Neuro‐anatomical differences among epileptic and non‐epileptic déjà‐vu. Cortex, 64, 1–7. 10.1016/j.cortex.2014.09.020 PubMed DOI

Lindauer, R. J. L. , Vlieger, E.‐J. , Jalink, M. , Olff, M. , Carlier, I. V. E. , Majoie, C. B. L. M. , … Gersons, B. P. R. (2005). Effects of psychotherapy on hippocampal volume in out‐patients with post‐traumatic stress disorder: A MRI investigation. Psychological Medicine, 35, 1421–1431. 10.1017/S0033291705005246 PubMed DOI

Lodge, D. J. , & Grace, A. A. (2011). Hippocampal dysregulation of dopamine system function and the pathophysiology of schizophrenia. Trends in Pharmacological Sciences, 32, 507–513. 10.1016/j.tips.2011.05.001 PubMed DOI PMC

Magariños, A. M. , Verdugo, J. M. , & McEwen, B. S. (1997). Chronic stress alters synaptic terminal structure in hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 94, 14002–14008. 10.1073/pnas.94.25.14002 PubMed DOI PMC

Malaeb, S. N. , Davis, J. M. , Pinz, I. M. , Newman, J. L. , Dammann, O. , & Rios, M. (2014). Effect of sustained postnatal systemic inflammation on hippocampal volume and function in mice. Pediatric Research, 76, 363–369. 10.1038/pr.2014.106 PubMed DOI PMC

Mamah, D. , Harms, M. P. , Barch, D. , Styner, M. , Lieberman, J. A. , & Wang, L. (2012). Hippocampal shape and volume changes with antipsychotics in early stage psychotic illness. Frontiers in Psychiatry, 3, 96 10.3389/fpsyt.2012.00096 PubMed DOI PMC

Marsland, A. L. , Gianaros, P. J. , Kuan, D. C.‐H. , Sheu, L. K. , Krajina, K. , & Manuck, S. B. (2015). Brain morphology links systemic inflammation to cognitive function in midlife adults. Brain, Behavior, and Immunity, 48, 195–204. 10.1016/j.bbi.2015.03.015 PubMed DOI PMC

Mathern, G. W. , Babb, T. L. , Leite, J. P. , Pretorius, K. , Yeoman, K. M. , & Kuhlman, P. A. (1996). The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Research, 26, 151–161. 10.1016/S0920-1211(96)00052-6 PubMed DOI

Mathew, I. , Gardin, T. M. , Tandon, N. , Eack, S. , Francis, A. N. , Seidman, L. J. , … Keshavan, M. S. (2014). Medial temporal lobe structures and hippocampal subfields in psychotic disorders: Findings from the Bipolar‐Schizophrenia Network on Intermediate Phenotypes (B‐SNIP) study. JAMA Psychiatry, 71, 769–777. 10.1001/jamapsychiatry.2014.453 PubMed DOI

McEwen, B. S. (1999). Stress and hippocampal plasticity. Annual Review of Neuroscience, 22, 105–122. 10.1146/annurev.neuro.22.1.105 PubMed DOI

Novati, A. , Hulshof, H. J. , Koolhaas, J. M. , Lucassen, P. J. , & Meerlo, P. (2011). Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience, 190, 145–155. 10.1016/j.neuroscience.2011.06.027 PubMed DOI

O’Donovan, A. , Chao, L. L. , Paulson, J. , Samuelson, K. W. , Shigenaga, J. K. , Grunfeld, C. , … Neylan, T. C. (2015). Altered inflammatory activity associated with reduced hippocampal volume and more severe posttraumatic stress symptoms in Gulf War veterans. Psychoneuroendocrinology, 51, 557–566. 10.1016/j.psyneuen.2014.11.010 PubMed DOI PMC

Pail, M. , Brázdil, M. , Mareček, R. , & Mikl, M. (2010). An optimized voxel‐based morphometric study of gray matter changes in patients with left‐sided and right‐sided mesial temporal lobe epilepsy and hippocampal sclerosis (MTLE/HS). Epilepsia, 51, 511–518. 10.1111/j.1528-1167.2009.02324.x PubMed DOI

Panenka, W. J. , Khorram, B. , Barr, A. M. , Smith, G. N. , Lang, D. J. , Kopala, L. C. , … Honer, W. G. (2007). A longitudinal study on the effects of typical versus atypical antipsychotic drugs on hippocampal volume in schizophrenia. Schizophrenia Research, 94, 288–292. 10.1016/j.schres.2007.05.002 PubMed DOI

Pavlides, C. , Watanabe, Y. , & McEwen, B. S. (1993). Effects of glucocorticoids on hippocampal long‐term potentiation. Hippocampus, 3, 183–192. 10.1002/hipo.450030210 PubMed DOI

Penfield, W. (1955). The twenty‐ninth Maudsley lecture: The role of the temporal cortex in certain psychical phenomena. The Journal of Mental Science, 101, 451–465. 10.1192/bjp.101.424.451 PubMed DOI

Richardson, T. F. , & Winokur, G. (1967). Déjà vu in psychiatric and neurosurgical patients. Archives of General Psychiatry, 17, 622–625. 10.1001/archpsyc.1967.01730290110014 PubMed DOI

Sapolsky, R. M. (1996). Stress, glucocorticoids, and damage to the nervous system: The current state of confusion. Stress: The International Journal on the Biology of Stress, 1, 1–19. 10.3109/10253899609001092 PubMed DOI

Schoene‐Bake, J.‐C. , Keller, S. S. , Niehusmann, P. , Volmering, E. , Elger, C. , Deppe, M. , & Weber, B. (2014). In vivo mapping of hippocampal subfields in mesial temporal lobe epilepsy: Relation to histopathology: Hippocampal Subfield Mapping in mTLE. Human Brain Mapping, 35, 4718–4728. 10.1002/hbm.22506 PubMed DOI PMC

Shaw, D. J. , Mareček, R. , & Brázdil, M. (2015). Structural covariance mapping delineates medial and medio‐lateral temporal networks in déjà vu. Brain Imaging and Behavior, 10.1007/s11682-015-9471-8 PubMed DOI

Sno, H. N. , Schalken, H. F. , de Jonghe, F. , & Koeter, M. W. (1994). The inventory for déjà vu experiences assessment. Development, utility, reliability, and validity. The Journal of Nervous and Mental Disease, 182, 27–33. 10.1097/00005053-199401000-00006 PubMed DOI

Tamminga, C. A. , Stan, A. D. , & Wagner, A. D. (2010). The hippocampal formation in schizophrenia. American Journal of Psychiatry, 167, 1178–1193. 10.1176/appi.ajp.2010.09081187 PubMed DOI

Tasch, E. , Cendes, F. , Li, L. M. , Dubeau, F. , Andermann, F. , & Arnold, D. L. (1999). Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Annals of Neurology, 45, 568–576. 10.1002/(ISSN)1531-8249 PubMed DOI

Teicher, M. H. , Anderson, C. M. , & Polcari, A. (2012). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proceedings of the National Academy of Sciences, 109, E563–E572. 10.1073/pnas.1115396109 PubMed DOI PMC

Thom, M. , Zhou, J. , Martinian, L. , & Sisodiya, S. (2005). Quantitative post‐mortem study of the hippocampus in chronic epilepsy: Seizures do not inevitably cause neuronal loss. Brain: A Journal of Neurology, 128, 1344–1357. 10.1093/brain/awh475 PubMed DOI

Walker, M. A. , Highley, J. R. , Esiri, M. M. , McDonald, B. , Roberts, H. C. , Evans, S. P. , & Crow, T. J. (2002). Estimated neuronal populations and volumes of the hippocampus and its subfields in schizophrenia. American Journal of Psychiatry, 159, 821–828. 10.1176/appi.ajp.159.5.821 PubMed DOI

Wang, L. , Mamah, D. , Harms, M. P. , Karnik, M. , Price, J. L. , Gado, M. H. , … Csernansky, J. G. (2008). Progressive deformation of deep brain nuclei and hippocampal‐amygdala formation in schizophrenia. Biological Psychiatry, 64, 1060–1068. 10.1016/j.biopsych.2008.08.007 PubMed DOI PMC

Wang, Z. , Neylan, T. C. , Mueller, S. G. , Lenoci, M. , Truran, D. , Marmar, C. R. , … Schuff, N. (2010). Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder. Archives of General Psychiatry, 67, 296–303. 10.1001/archgenpsychiatry.2009.205 PubMed DOI PMC

Warren‐Gash, C. , & Zeman, A. (2014). Is there anything distinctive about epileptic deja vu? Journal of Neurology, Neurosurgery and Psychiatry, 85, 143–147. 10.1136/jnnp-2012-303520 PubMed DOI

Weiss, A. P. , Schacter, D. L. , Goff, D. C. , Rauch, S. L. , Alpert, N. M. , Fischman, A. J. , & Heckers, S. (2003). Impaired hippocampal recruitment during normal modulation of memory performance in schizophrenia. Biological Psychiatry, 53, 48–55. 10.1016/S0006-3223(02)01541-X PubMed DOI

Zierhut, K. C. , Graßmann, R. , Kaufmann, J. , Steiner, J. , Bogerts, B. , & Schiltz, K. (2013). Hippocampal CA1 deformity is related to symptom severity and antipsychotic dosage in schizophrenia. Brain: A Journal of Neurology, 136, 804–814. 10.1093/brain/aws335 PubMed DOI