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Interictal psychosis following temporal lobe surgery: dentate gyrus pathology

Published online by Cambridge University Press:  08 April 2014

M. Thom ,
M. Kensche ,
J. Maynard ,
J. Liu ,
C. Reeves ,
J. Goc ,
D. Marsdon ,
D. Fluegel  and
J. Foong
M. Thom*
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK Division of Neuropathology, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK
M. Kensche
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK Division of Neuropsychiatry, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK
J. Maynard
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK Division of Neuropathology, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK
J. Liu
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK
C. Reeves
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK
J. Goc
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK
D. Marsdon
Affiliation:
Division of Neuropathology, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK
D. Fluegel
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK Division of Neuropsychiatry, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK
J. Foong
Affiliation:
Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, London, UK Division of Neuropsychiatry, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK
*
*Address for correspondence: M. Thom, Ph.D., Department of Clinical and Experimental Epilepsy, University College London, Institute of Neurology, Queen Square, London WC1N 3BG, UK. (Email: M.Thom@ucl.ac.uk)
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Abstract

Background

De novo interictal psychosis, albeit uncommon, can develop in patients following temporal lobe surgery for epilepsy. Pathological alterations of the dentate gyrus, including cytoarchitectural changes, immaturity and axonal reorganization that occur in epilepsy, may also underpin co-morbid psychiatric disorders. Our aim was to study candidate pathways that may be associated with the development of interictal psychosis post-operatively in patients with hippocampal sclerosis (HS).

Method

A total of 11 patients with HS who developed interictal psychosis (HS-P) post-operatively were compared with a matched surgical HS group without psychosis (HS-NP). Resected tissues were investigated for the extent of granule cell dispersion, mossy fibre sprouting and calbindin expression in the granule cells. We quantified doublecortin, mini-chromosome maintenance protein 2 (MCM2) and reelin-expressing neuronal populations in the dentate gyrus as well as the distribution of cannabinoid type 1 receptor (CBR1).

Results

The patterns of neuronal loss and gliosis were similar in both groups. HS-P patients demonstrated less mossy fibre sprouting and granule cell dispersion (p < 0.01) and more frequent reduction in calbindin expression in granule cells. There were no group differences in the densities of immature MCM2, doublecortin and reelin-positive cells. CBR1 labelling was significantly lower in Cornu ammonis area CA4 relative to other subfields (p < 0.01); although reduced staining in all hippocampal regions was noted in HS-P compared with HS-NP patients, the differences were not statistically significant.

Conclusions

The alterations in dentate gyrus pathology found in HS-P patients could indicate underlying differences in the cellular response to seizures. These mechanisms may predispose to the development of psychosis in epilepsy and warrant further investigation.

Keywords

Dentate gyrusepilepsyhippocampal sclerosispsychosis
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 14 , October 2014 , pp. 3037 - 3049
Copyright
Copyright © Cambridge University Press 2014 

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References

Abraham, H, Meyer, G (2003). Reelin-expressing neurons in the postnatal and adult human hippocampal formation. Hippocampus 13, 715–727.Google Scholar
Abraham, H, Richter, Z, Gyimesi, C, Horvath, Z, Janszky, J, Doczi, T, Seress, L (2011). Degree and pattern of calbindin immunoreactivity in granule cells of the dentate gyrus differ in mesial temporal sclerosis, cortical malformation- and tumor-related epilepsies. Brain Research 1399, 66–78.Google Scholar
Altar, CA, Jurata, LW, Charles, V, Lemire, A, Liu, P, Bukhman, Y, Young, TA, Bullard, J, Yokoe, H, Webster, MJ, Knable, MB, Brockman, JA (2005). Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts. Biological Psychiatry 58, 85–96.Google Scholar
Andermann, LF, Savard, G, Meencke, HJ, McLachlan, R, Moshe, S, Andermann, F (1999). Psychosis after resection of ganglioglioma or DNET: evidence for an association. Epilepsia 40, 83–87.Google Scholar
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, text-revision. American Psychological Association: Washington, DC.Google Scholar
Arellano, JI, Munoz, A, Ballesteros-Yanez, I, Sola, RG, DeFelipe, J (2004). Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain 127, 45–64.Google Scholar
Ben-David, E, Shifman, S (2010). Further investigation of the association between rs7341475 and rs17 746 501 and schizophrenia. Americal Journal of Medical Genetics, Part B Neuropsychiatric Genetics 153B, 1244–1247.Google Scholar
Blumcke, I (2009). Neuropathology of focal epilepsies: a critical review. Epilepsy Behaviour 15, 34–39.Google Scholar
Blumcke, I, Coras, R, Miyata, H, Ozkara, C (2012). Defining clinico-neuropathological subtypes of mesial temporal lobe epilepsy with hippocampal sclerosis. Brain Pathology 22, 402–411.CrossRefGoogle ScholarPubMed
Blumcke, I, Kistner, I, Clusmann, H, Schramm, J, Becker, AJ, Elger, CE, Bien, CG, Merschhemke, M, Meencke, HJ, Lehmann, T, Buchfelder, M, Weigel, D, Buslei, R, Stefan, H, Pauli, E, Hildebrandt, M (2009). Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathologica 117, 535–544.CrossRefGoogle ScholarPubMed
Blumcke, I, Thom, M, Aronica, E, Armstrong, DD, Bartolomei, F, Bernasconi, A, Bernasconi, N, Bien, CG, Cendes, F, Coras, R, Cross, JH, Jacques, TS, Kahane, P, Mathern, GW, Miyata, H, Moshe, SL, Oz, B, Ozkara, C, Perucca, E, Sisodiya, S, Wiebe, S, Spreafico, R (2013). International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia 54, 1315–1329.Google Scholar
Briellmann, RS, Kalnins, RM, Hopwood, MJ, Ward, C, Berkovic, SF, Jackson, GD (2000). TLE patients with postictal psychosis: mesial dysplasia and anterior hippocampal preservation. Neurology 55, 1027–1030.Google Scholar
Cameron, MC, Zhan, RZ, Nadler, JV (2011). Morphologic integration of hilar ectopic granule cells into dentate gyrus circuitry in the pilocarpine model of temporal lobe epilepsy. Journal of Comparative Neurology 519, 2175–2192.Google Scholar
Chai, X, Munzner, G, Zhao, S, Tinnes, S, Kowalski, J, Haussler, U, Young, C, Haas, CA, Frotscher, M (2013). Epilepsy-induced motility of differentiated neurons. Cerebral Cortex. Published online 15 March 2013 . doi:10.1093/cercor/bht067.Google Scholar
Chavarria-Siles, I, Contreras-Rojas, J, Hare, E, Walss-Bass, C, Quezada, P, Dassori, A, Contreras, S, Medina, R, Ramirez, M, Salazar, R, Raventos, H, Escamilla, MA (2008). Cannabinoid receptor 1 gene (CNR1) and susceptibility to a quantitative phenotype for hebephrenic schizophrenia. American Journal of Medical Genetics Part B Neuropsychiatric Genetics 147, 279–284.Google Scholar
Choi, H, Sell, RL, Lenert, L, Muennig, P, Goodman, RR, Gilliam, FG, Wong, JB (2008). Epilepsy surgery for pharmacoresistant temporal lobe epilepsy: a decision analysis. Journal of the American Medical Association 300, 2497–2505.CrossRefGoogle ScholarPubMed
Christodoulou, C, Koutroumanidis, M, Hennessy, MJ, Elwes, RD, Polkey, CE, Toone, BK (2002). Postictal psychosis after temporal lobectomy. Neurology 59, 1432–1435.Google Scholar
Cleary, RA, Thompson, PJ, Fox, Z, Foong, J (2012). Predictors of psychiatric and seizure outcome following temporal lobe epilepsy surgery. Epilepsia 53, 1705–1712.Google Scholar
Coras, R, Siebzehnrubl, FA, Pauli, E, Huttner, HB, Njunting, M, Kobow, K, Villmann, C, Hahnen, E, Neuhuber, W, Weigel, D, Buchfelder, M, Stefan, H, Beck, H, Steindler, DA, Blumcke, I (2010). Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans. Brain 133, 3359–3372.Google Scholar
Cotter, D, Wilson, S, Roberts, E, Kerwin, R, Everall, IP (2000). Increased dendritic MAP2 expression in the hippocampus in schizophrenia. Schizophrenia Research 41, 313–323.Google Scholar
D'Alessio, L, Konopka, H, Lopez, EM, Seoane, E, Consalvo, D, Oddo, S, Kochen, S, Lopez-Costa, JJ (2010). Doublecortin (DCX) immunoreactivity in hippocampus of chronic refractory temporal lobe epilepsy patients with hippocampal sclerosis. Seizure 19, 567–572.Google Scholar
Dean, B, Sundram, S, Bradbury, R, Scarr, E, Copolov, D (2001). Studies on [3H]CP-55940 binding in the human central nervous system: regional specific changes in density of cannabinoid-1 receptors associated with schizophrenia and cannabis use. Neuroscience 103, 9–15.CrossRefGoogle ScholarPubMed
Eastwood, SL, Harrison, PJ (2006). Cellular basis of reduced cortical reelin expression in schizophrenia. American Journal of Psychiatry 163, 540–542.Google Scholar
Enomoto, A, Asai, N, Namba, T, Wang, Y, Kato, T, Tanaka, M, Tatsumi, H, Taya, S, Tsuboi, D, Kuroda, K, Kaneko, N, Sawamoto, K, Miyamoto, R, Jijiwa, M, Murakumo, Y, Sokabe, M, Seki, T, Kaibuchi, K, Takahashi, M (2009). Roles of disrupted-in-schizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron 63, 774–787.Google Scholar
Fahrner, A, Kann, G, Flubacher, A, Heinrich, C, Freiman, TM, Zentner, J, Frotscher, M, Haas, CA (2007). Granule cell dispersion is not accompanied by enhanced neurogenesis in temporal lobe epilepsy patients. Experimental Neurology 203, 320–332.CrossRefGoogle Scholar
Fatemi, SH (2005). Reelin glycoprotein in autism and schizophrenia. International Review of Neurobiology 71, 179–187.Google Scholar
Fernandez-Espejo, E, Viveros, MP, Nunez, L, Ellenbroek, BA, Rodriguez de Fonseca, F (2009). Role of cannabis and endocannabinoids in the genesis of schizophrenia. Psychopharmacology (Berlin) 206, 531–549.Google Scholar
Flor-Henry, P (1969). Psychosis and temporal lobe epilepsy. A controlled investigation. Epilepsia 10, 363–395.CrossRefGoogle ScholarPubMed
Flugel, D, Cercignani, M, Symms, MR, Koepp, MJ, Foong, J (2006). A magnetization transfer imaging study in patients with temporal lobe epilepsy and interictal psychosis. Biological Psychiatry 59, 560–567.Google Scholar
Folsom, TD, Fatemi, SH (2013). The involvement of reelin in neurodevelopmental disorders. Neuropharmacology 68, 122–135.CrossRefGoogle ScholarPubMed
Foong, J, Flugel, D (2007). Psychiatric outcome of surgery for temporal lobe epilepsy and presurgical considerations. Epilepsy Research 75, 84–96.Google Scholar
Frotscher, M, Haas, CA, Förster, E (2003). Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cerebral Cortex 13, 634–640.Google Scholar
Garey, L (2010). When cortical development goes wrong: schizophrenia as a neurodevelopmental disease of microcircuits. Journal of Anatomy 217, 324–333.Google Scholar
Glosser, G, Zwil, AS, Glosser, DS, O'Connor, MJ, Sperling, MR (2000). Psychiatric aspects of temporal lobe epilepsy before and after anterior temporal lobectomy. Journal of Neurology, Neurosurgery and Psychiatry 68, 53–58.Google Scholar
Goffin, K, Van Paesschen, W, Van Laere, K (2011). In vivo activation of endocannabinoid system in temporal lobe epilepsy with hippocampal sclerosis. Brain 134, 1033–1040.Google Scholar
Haas, CA, Frotscher, M (2010). Reelin deficiency causes granule cell dispersion in epilepsy. Experimental Brain Research 200, 141–149.CrossRefGoogle ScholarPubMed
Habl, G, Schmitt, A, Zink, M, von Wilmsdorff, M, Yeganeh-Doost, P, Jatzko, A, Schneider-Axmann, T, Bauer, M, Falkai, P (2012). Decreased reelin expression in the left prefrontal cortex (BA9) in chronic schizophrenia patients. Neuropsychobiology 66, 57–62.Google Scholar
Hamdani, N, Tabeze, JP, Ramoz, N, Ades, J, Hamon, M, Sarfati, Y, Boni, C, Gorwood, P (2008). The CNR1 gene as a pharmacogenetic factor for antipsychotics rather than a susceptibility gene for schizophrenia. European Neuropsychopharmacology 18, 34–40.Google Scholar
Heck, N, Garwood, J, Loeffler, JP, Larmet, Y, Faissner, A (2004). Differential upregulation of extracellular matrix molecules associated with the appearance of granule cell dispersion and mossy fiber sprouting during epileptogenesis in a murine model of temporal lobe epilepsy. Neuroscience 129, 309–324.CrossRefGoogle Scholar
Hussain, ZM, Fitting, S, Watanabe, H, Usynin, I, Yakovleva, T, Knapp, PE, Scheff, SW, Hauser, KF, Bakalkin, G (2012). Lateralized response of dynorphin A peptide levels after traumatic brain injury. Journal of Neurotrauma 29, 1785–1793.Google Scholar
Impagnatiello, F, Guidotti, AR, Pesold, C, Dwivedi, Y, Caruncho, H, Pisu, MG, Uzunov, DP, Smalheiser, NR, Davis, JM, Pandey, GN, Pappas, GD, Tueting, P, Sharma, RP, Costa, E (1998). A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proceedings of the National Academy of Sciences USA 95, 15718–15723.Google Scholar
Inoue, Y, Mihara, T (2001). Psychiatric disorders before and after surgery for epilepsy. Epilepsia 42 (Suppl. 6), 13–18.Google Scholar
Kandratavicius, L, Hallak, JE, Young, LT, Assirati, JA, Carlotti, CG Jr., Leite, JP (2012). Differential aberrant sprouting in temporal lobe epilepsy with psychiatric co-morbidities. Psychiatry Research 195, 144–150.Google Scholar
Kanner, AM, Byrne, R, Chicharro, A, Wuu, J, Frey, M (2009). A lifetime psychiatric history predicts a worse seizure outcome following temporal lobectomy. Neurology 72, 793–799.Google Scholar
Karadi, K, Janszky, J, Gyimesi, C, Horvath, Z, Lucza, T, Doczi, T, Kallai, J, Abraham, H (2012). Correlation between calbindin expression in granule cells of the resected hippocampal dentate gyrus and verbal memory in temporal lobe epilepsy. Epilepsy Behaviour 25, 110–119.Google Scholar
Karlocai, MR, Toth, K, Watanabe, M, Ledent, C, Juhasz, G, Freund, TF, Magloczky, Z (2011). Redistribution of CB1 cannabinoid receptors in the acute and chronic phases of pilocarpine-induced epilepsy. PloS ONE 6, e27196.CrossRefGoogle ScholarPubMed
Katona, I, Freund, TF (2008). Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nature Medicine 14, 923–930.CrossRefGoogle ScholarPubMed
Katona, I, Freund, TF (2012). Multiple functions of endocannabinoid signaling in the brain. Annual Review of Neuroscience 35, 529–558.Google Scholar
Kirov, II, Hardy, CJ, Matsuda, K, Messinger, J, Cankurtaran, CZ, Warren, M, Wiggins, GC, Perry, NN, Babb, JS, Goetz, RR, George, A, Malaspina, D, Gonen, O (2013). In vivo 7 Tesla imaging of the dentate granule cell layer in schizophrenia. Schizophrenia Research 147, 362–367.CrossRefGoogle ScholarPubMed
Knable, MB, Barci, BM, Webster, MJ, Meador-Woodruff, J, Torrey, EF (2004). Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Molecular Psychiatry 9, 609–620.Google Scholar
Koyama, R, Tao, K, Sasaki, T, Ichikawa, J, Miyamoto, D, Muramatsu, R, Matsuki, N, Ikegaya, Y (2012). GABAergic excitation after febrile seizures induces ectopic granule cells and adult epilepsy. Nature Medicine 18, 1271–1278.CrossRefGoogle ScholarPubMed
Kuang, WJ, Sun, RF, Zhu, YS, Li, SB (2011). A new single-nucleotide mutation (rs362719) of the reelin (RELN) gene associated with schizophrenia in female Chinese Han. Genetetics and Molecular Research 10, 1650–1658.CrossRefGoogle ScholarPubMed
Lakatosova, S, Ostatnikova, D (2012). Reelin and its complex involvement in brain development and function. International Journal of Biochemistry and Cell Biology 44, 1501–1504.Google Scholar
Leinonen, E, Tuunainen, A, Lepola, U (1994). Postoperative psychoses in epileptic patients after temporal lobectomy. Acta Neurologica Scandinavica 90, 394–399.Google Scholar
Lindsay, J, Ounsted, C, Richards, P (1979). Long-term outcome in children with temporal lobe seizures. III: Psychiatric aspects in childhood and adult life. Developmental Medicine and Child Neurology 21, 630–636.Google Scholar
Ludanyi, A, Eross, L, Czirjak, S, Vajda, J, Halasz, P, Watanabe, M, Palkovits, M, Magloczky, Z, Freund, TF, Katona, I (2008). Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. Journal of Neuroscience 28, 2976–2990.Google Scholar
Luzi, S, Morrison, PD, Powell, J, di Forti, M, Murray, RM (2008). What is the mechanism whereby cannabis use increases risk of psychosis? Neurotoxicity Research 14, 105–112.Google Scholar
Mace, CJ, Trimble, MR (1991). Psychosis following temporal lobe surgery: a report of six cases. Journal of Neurology, Neurosurgery and Psychiatry 54, 639–644.Google Scholar
Magloczky, Z, Halasz, P, Vajda, J, Czirjak, S, Freund, TF (1997). Loss of calbindin-D28 K immunoreactivity from dentate granule cells in human temporal lobe epilepsy. Neuroscience 76, 377–385.Google Scholar
Magloczky, Z, Toth, K, Karlocai, R, Nagy, S, Eross, L, Czirjak, S, Vajda, J, Rasonyi, G, Kelemen, A, Juhos, V, Halasz, P, Mackie, K, Freund, TF (2010). Dynamic changes of CB1-receptor expression in hippocampi of epileptic mice and humans. Epilepsia 51 (Suppl. 3), 115–120.Google Scholar
Maier, M, Mellers, J, Toone, B, Trimble, M, Ron, MA (2000). Schizophrenia, temporal lobe epilepsy and psychosis: an in vivo magnetic resonance spectroscopy and imaging study of the hippocampus/amygdala complex. Psychological Medicine 30, 571–581.Google Scholar
Manchanda, R, Miller, H, McLachlan, RS (1993). Post-ictal psychosis after right temporal lobectomy. Journal of Neurology, Neurosurgery and Psychiatry 56, 277–279.Google Scholar
Marshall, EJ, Syed, GM, Fenwick, PB, Lishman, WA (1993). A pilot study of schizophrenia-like psychosis in epilepsy using single-photon emission computerised tomography. British Journal of Psychiatry 163, 32–36.Google Scholar
Martinian, L, Boer, K, Middeldorp, J, Hol, EM, Sisodiya, SM, Squier, W, Aronica, E, Thom, M (2009). Expression patterns of glial fibrillary acidic protein (GFAP)-delta in epilepsy-associated lesional pathologies. Neuropathology and Applied Neurobiology 35, 394–405.Google Scholar
Martinian, L, Catarino, CB, Thompson, P, Sisodiya, SM, Thom, M (2012). Calbindin D28 K expression in relation to granule cell dispersion, mossy fibre sprouting and memory impairment in hippocampal sclerosis: a surgical and post mortem series. Epilepsy Research 98, 14–24.Google Scholar
Mellers, JD, Adachi, N, Takei, N, Cluckie, A, Toone, BK, Lishman, WA (1998). SPET study of verbal fluency in schizophrenia and epilepsy. British Journal of Psychiatry 173, 69–74.Google Scholar
Monory, K, Massa, F, Egertova, M, Eder, M, Blaudzun, H, Westenbroek, R, Kelsch, W, Jacob, W, Marsch, R, Ekker, M, Long, J, Rubenstein, JL, Goebbels, S, Nave, KA, During, M, Klugmann, M, Wolfel, B, Dodt, HU, Zieglgansberger, W, Wotjak, CT, Mackie, K, Elphick, MR, Marsicano, G, Lutz, B (2006). The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51, 455–466.Google Scholar
Nadkarni, S, Arnedo, V, Devinsky, O (2007). Psychosis in epilepsy patients. Epilepsia 48 (Suppl. 9), 17–19.Google Scholar
Nadler, JV (2003). The recurrent mossy fiber pathway of the epileptic brain. Neurochemistry Research 28, 1649–1658.CrossRefGoogle ScholarPubMed
Paine, S, Willsher, A, Nicholson, S, Sebire, N, Jacques, T (2013). Characterisation of a population of neural progenitor cells in the infant hippocampus. Neuropathology and Applied Neurobiology. Published online 6 June 2013 . doi:10.1111/nan.12065.Google Scholar
Perez, MM, Trimble, MR (1980). Epileptic psychosis–diagnostic comparison with process schizophrenia. British Journal of Psychiatry 137, 245–249.Google Scholar
Proper, EA, Jansen, GH, van Veelen, CW, van Rijen, PC, Gispen, WH, de Graan, PN (2001). A grading system for hippocampal sclerosis based on the degree of hippocampal mossy fiber sprouting. Acta Neuropathologica 101, 405–409.Google Scholar
Radhakrishnan, A, Radhakrishnan, K, Radhakrishnan, VV, Mary, PR, Kesavadas, C, Alexander, A, Sarma, PS (2007). Corpora amylacea in mesial temporal lobe epilepsy: clinico-pathological correlations. Epilepsy Research 74, 81–90.Google Scholar
Reif, A, Fritzen, S, Finger, M, Strobel, A, Lauer, M, Schmitt, A, Lesch, KP (2006). Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Molecular Psychiatry 11, 514–522.Google Scholar
Roberts, GW, Done, DJ, Bruton, C, Crow, TJ (1990). A “mock up” of schizophrenia: temporal lobe epilepsy and schizophrenia-like psychosis. Biological Psychiatry 28, 127–143.Google Scholar
Rosoklija, G, Toomayan, G, Ellis, SP, Keilp, J, Mann, JJ, Latov, N, Hays, AP, Dwork, AJ (2000). Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Archives of General Psychiatry 57, 349–356.Google Scholar
Shaw, P, Mellers, J, Henderson, M, Polkey, C, David, AS, Toone, BK (2004). Schizophrenia-like psychosis arising de novo following a temporal lobectomy: timing and risk factors. Journal of Neurology, Neurosurgery and Psychiatry 75, 1003–1008.Google Scholar
Shin, R, Kobayashi, K, Hagihara, H, Kogan, JH, Miyake, S, Tajinda, K, Walton, NM, Gross, AK, Heusner, CL, Chen, Q, Tamura, K, Miyakawa, T, Matsumoto, M (2013). The immature dentate gyrus represents a shared phenotype of mouse models of epilepsy and psychiatric disease. Bipolar Disorder. Published online 6 April 2013 . doi:10.1111/bdi.12064.Google Scholar
Stevens, JR (1990). Psychiatric consequences of temporal lobectomy for intractable seizures: a 20–30-year follow-up of 14 cases. Psychologcal Medicine 20, 529–545.Google Scholar
Stranahan, AM, Erion, JR, Wosiski-Kuhn, M (2013). Reelin signaling in development, maintenance, and plasticity of neural networks. Ageing Research Reviews 12, 815–822.Google Scholar
Suckling, J, Roberts, H, Walker, M, Highley, JR, Fenwick, P, Oxbury, J, Esiri, MM (2000). Temporal lobe epilepsy with and without psychosis: exploration of hippocampal pathology including that in subpopulations of neurons defined by their content of immunoreactive calcium-binding proteins. Acta Neuropathologica 99, 547–554.Google Scholar
Sutula, T, Cascino, G, Cavazos, J, Parada, I, Ramirez, L (1989). Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Annals of Neurology 26, 321–330.Google Scholar
Tamminga, CA, Stan, AD, Wagner, AD (2010). The hippocampal formation in schizophrenia. American Journal of Psychiatry 167, 1178–1193.Google Scholar
Thom, M, Liagkouras, I, Elliot, KJ, Martinian, L, Harkness, W, McEvoy, A, Caboclo, LO, Sisodiya, SM (2010). Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 51, 1801–1808.Google Scholar
Thom, M, Martinian, L, Catarino, C, Yogarajah, M, Koepp, MJ, Caboclo, L, Sisodiya, SM (2009). Bilateral reorganization of the dentate gyrus in hippocampal sclerosis: a postmortem study. Neurology 73, 1033–1040.Google Scholar
Thom, M, Martinian, L, Sisodiya, SM, Cross, JH, Williams, G, Stoeber, K, Harkness, W, Harding, BN (2005 a). Mcm2 labelling of balloon cells in focal cortical dysplasia. Neuropathology and Applied Neurobiology 31, 580–588.Google Scholar
Thom, M, Martinian, L, Williams, G, Stoeber, K, Sisodiya, SM (2005 b). Cell proliferation and granule cell dispersion in human hippocampal sclerosis. Journal of Neuropathology and Experimental Neurology 64, 194–201.Google Scholar
Thom, M, Sisodiya, SM, Beckett, A, Martinian, L, Lin, WR, Harkness, W, Mitchell, TN, Craig, J, Duncan, J, Scaravilli, F (2002). Cytoarchitectural abnormalities in hippocampal sclerosis. Journal of Neuropathology and Experimental Neurology 61, 510–519.CrossRefGoogle ScholarPubMed
Toone, BK (2000). The psychoses of epilepsy. Journal of Neurology, Neurosurgery and Psychiatry 69, 1–3.Google Scholar
Trimble, M (1992). Neurological models of schizophrenia – regional implications. Clinical Neuropharmacology 15 (Suppl. 1 Pt. A), 395A–396A.Google Scholar
Ujike, H, Morita, Y (2004). New perspectives in the studies on endocannabinoid and cannabis: cannabinoid receptors and schizophrenia. Journal of Pharmacological Science 96, 376–381.Google Scholar
von Bohlen und Halbach, O (2011). Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Research 345, 1–19.Google Scholar
Walton, NM, Zhou, Y, Kogan, JH, Shin, R, Webster, M, Gross, AK, Heusner, CL, Chen, Q, Miyake, S, Tajinda, K, Tamura, K, Miyakawa, T, Matsumoto, M (2012). Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients. Translational Psychiatry 2, e135.Google Scholar
Wong, DF, Kuwabara, H, Horti, AG, Raymont, V, Brasic, J, Guevara, M, Ye, W, Dannals, RF, Ravert, HT, Nandi, A, Rahmim, A, Ming, JE, Grachev, I, Roy, C, Cascella, N (2010). Quantification of cerebral cannabinoid receptors subtype 1 (CB1) in healthy subjects and schizophrenia by the novel PET radioligand [11C]OMAR. NeuroImage 52, 1505–1513.Google Scholar
Zavitsanou, K, Garrick, T, Huang, XF (2004). Selective antagonist [3H]SR141 716A binding to cannabinoid CB1 receptors is increased in the anterior cingulate cortex in schizophrenia. Progress in Neuropsychopharmacology and Biological Psychiatry 28, 355–360.Google Scholar
Zhang, ZJ, Reynolds, GP (2002). A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophrenia Research 55, 1–10.Google Scholar