Table of Contents Author Guidelines Submit a Manuscript
Neuroscience Journal
Volume 2018, Article ID 4852359, 9 pages
https://doi.org/10.1155/2018/4852359
Review Article

Hippocampal Pathophysiology: Commonality Shared by Temporal Lobe Epilepsy and Psychiatric Disorders

1Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, CA 92617, USA
2Candidate Discovery Science Labs, Drug Discovery Research, Astellas Pharma Inc., 21 Miyukigaoka, Tsukuba, Ibaraki 305-8585, Japan
3Neuroscience, La Jolla Laboratory Astellas Research Institute of America, LLC. 3565 General Atomics Court, Suite 200, San Diego, CA 92121, USA

Correspondence should be addressed to Soichiro Nakahara; ude.icu@srahakan

Received 5 October 2017; Revised 2 December 2017; Accepted 20 December 2017; Published 22 January 2018

Academic Editor: Pasquale Striano

Copyright © 2018 Soichiro Nakahara et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. M. Hyde and D. R. Weinberger, “Seizures and schizophrenia,” Schizophrenia Bulletin, vol. 23, no. 4, pp. 611–622, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. J. M. Gold, B. P. Hermann, C. Randolph, A. R. Wyler, T. E. Goldberg, and D. R. Weinberger, “Schizophrenia and temporal lobe epilepsy. A neuropsychological analysis,” Archives of General Psychiatry, vol. 51, no. 4, pp. 265–272, 1994. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Kandratavicius, C. Lopes-Aguiar, L. S. Bueno-Júnior, R. N. Romcy-Pereira, J. E. C. Hallak, and J. P. Leite, “Psychiatric comorbidities in temporal lobe epilepsy: possible relationships between psychotic disorders and involvement of limbic circuits,” Revista Brasileira de Psiquiatria, vol. 34, no. 4, pp. 454–466, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. A. B. Ettinger, M. L. Reed, J. F. Goldberg, and R. M. A. Hirschfeld, “Prevalence of bipolar symptoms in epilepsy vs other chronic health disorders,” Neurology, vol. 65, no. 4, pp. 535–540, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Lau, A. B. Ettinger, S. Hamberger, K. Fanning, and M. L. Reed, “Do mood instability symptoms in epilepsy represent formal bipolar disorder?” Epilepsia, vol. 53, no. 2, pp. e37–e40, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. M. C. Clarke, A. Tanskanen, M. O. Huttunen, M. Clancy, D. R. Cotter, and M. Cannon, “Evidence for shared susceptibility to epilepsy and psychosis: a population-based family study,” Biological Psychiatry, vol. 71, no. 9, pp. 836–839, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Nishida, T. Kudo, Y. Inoue et al., “Postictal mania versus postictal psychosis: differences in clinical features, epileptogenic zone, and brain functional changes during postictal period,” Epilepsia, vol. 47, no. 12, pp. 2104–2114, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. P. B. Carrieri, V. Provitera, B. Iacovitti, C. Iachetta, C. Nappi, and A. Indaco, “Mood disorders in epilepsy,” Acta Neurochirurgica, vol. 15, no. 1, pp. 62–67, 1993. View at Google Scholar · View at Scopus
  9. M. Ito, “Neuropsychiatric evaluations of postictal behavioral changes,” Epilepsy & Behavior, vol. 19, no. 2, pp. 134–137, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Vuilleumier and P. Jallon, “Epilepsy and psychiatric disorders: epidemiological data,” Revue Neurologique, vol. 154, no. 4, pp. 305–317, 1998. View at Google Scholar · View at Scopus
  11. T. Mäkikyrö, J. T. Karvonen, H. Hakko et al., “Comorbidity of hospital-treated psychiatric and physical disorders with special reference to schizophrenia: a 28 year follow-up of the 1966 northern Finland general population birth cohort,” Public Health, vol. 112, no. 4, pp. 221–228, 1998. View at Google Scholar · View at Scopus
  12. D. P. Moreira, K. Griesi-Oliveira, A. L. Bossolani-Martins et al., “Investigation of 15q11-q13, 16p11.2 and 22q13 CNVs in autism spectrum disorder Brazilian individuals with and without epilepsy,” PLoS ONE, vol. 9, no. 9, Article ID e107705, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Ottman, R. B. Lipton, A. B. Ettinger et al., “Comorbidities of epilepsy: results from the Epilepsy Comorbidities and Health (EPIC) survey,” Epilepsia, vol. 52, no. 2, pp. 308–315, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. I. García-Morales, P. D. L. P. Mayor, and A. M. Kanner, “Psychiatric comorbidities in epilepsy: identification and treatment,” The Neurologist, vol. 14, supplementary 1, no. 6, pp. S15–S25, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. C. J. Wotton and M. J. Goldacre, “Record-linkage studies of the coexistence of epilepsy and bipolar disorder,” Social Psychiatry and Psychiatric Epidemiology, vol. 49, no. 9, pp. 1483–1488, 2014. View at Publisher · View at Google Scholar
  16. C. Adelöw, T. Andersson, A. Ahlbom, and T. Tomson, “Hospitalization for psychiatric disorders before and after onset of unprovoked seizures/epilepsy,” Neurology, vol. 78, no. 6, pp. 396–401, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. M. J. Clancy, M. C. Clarke, D. J. Connor, M. Cannon, and D. R. Cotter, “The prevalence of psychosis in epilepsy; a systematic review and meta-analysis,” BMC Psychiatry, vol. 14, article 75, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. W. A. Hauser, “The prevalence and incidence of convulsive disorders in children,” Epilepsia, vol. 35, pp. S1–S6, 1994. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Cendes, F. Andermann, F. Dubeau et al., “Early childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study,” Neurology, vol. 43, no. 6, pp. 1083–1087, 1993. View at Publisher · View at Google Scholar · View at Scopus
  20. J. A. French, P. D. Williamson, V. M. Thadani et al., “Characteristics of medial temporal lobe epilepsy: I. results of history and physical examination,” Annals of Neurology, vol. 34, no. 6, pp. 774–780, 1993. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Vestergaard, C. B. Pedersen, J. Christensen, K. M. Madsen, J. Olsen, and P. B. Mortensen, “Febrile seizures and risk of schizophrenia,” Schizophrenia Research, vol. 73, no. 2-3, pp. 343–349, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Hakyemez, K. Yucel, N. Yildirim, C. Erdogan, I. Bora, and M. Parlak, “Morphologic and volumetric analysis of amygdala, hippocampus, fornix and mamillary body with MRI in patients with temporal lobe epilepsy,” Neuroradiology, vol. 19, no. 3, pp. 289–296, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. M. C. Sandmann, E. Rogacheski, S. Mazer, and P. R. de Bittencourt, “Lateralization of the epileptogenic area by magnetic resonance imaging in temporal lobe epilepsy,” Arquivos de Neuro-Psiquiatria, vol. 52, no. 3, pp. 309–313, 1994. View at Publisher · View at Google Scholar · View at Scopus
  24. G. W. Roberts and C. J. Bruton, “Notes from the graveyard: neuropathology and schizophrenia,” Neuropathology and Applied Neurobiology, vol. 16, no. 1, pp. 3–16, 1990. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Heckers, “Neuroimaging studies of the hippocampus in schizophrenia,” Hippocampus, vol. 11, no. 5, pp. 520–528, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Cersósimo, S. Flesler, M. Bartuluchi, A. M. Soprano, H. Pomata, and R. Caraballo, “Mesial temporal lobe epilepsy with hippocampal sclerosis: study of 42 children,” Seizure, vol. 20, no. 2, pp. 131–137, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. P. A. Rutecki, R. G. Grossmann, D. Armstrong, and S. Irish-Loewen, “Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures,” Journal of Neurosurgery, vol. 70, no. 5, pp. 667–675, 1989. View at Publisher · View at Google Scholar · View at Scopus
  28. C. L. Wilson, M. Isokawa, T. L. Babb, and P. H. Crandall, “Functional connections in the human temporal lobe - I. Analysis of limbic system pathways using neuronal responses evoked by electrical stimulation,” Experimental Brain Research, vol. 82, no. 2, pp. 279–292, 1990. View at Publisher · View at Google Scholar · View at Scopus
  29. E. E. Krieckhaus, J. W. Donahoe, and M. A. Morgan, “Paranoid schizophrenia may be caused by dopamine hyperactivity of CA1 hippocampus,” Biological Psychiatry, vol. 31, no. 6, pp. 560–570, 1992. View at Publisher · View at Google Scholar · View at Scopus
  30. P. H. Venables, “Hippocampal function and schizophrenia. experimental psychological evidence,” Annals of the New York Academy of Sciences, vol. 658, no. 1, pp. 111–127, 1992. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Heckers and C. Konradi, “GABAergic mechanisms of hippocampal hyperactivity in schizophrenia,” Schizophrenia Research, vol. 167, no. 1-3, pp. 4–11, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Heckers, S. L. Rauch, D. Goff et al., “Impaired recruitment of the hippocampus during conscious recollection in schizophrenia,” Nature Neuroscience, vol. 1, no. 4, pp. 318–323, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. D. R. Medoff, H. H. Holcomb, A. C. Lahti, and C. A. Tamminga, “Probing the human hippocampus using rCBF: contrasts in schizophrenia,” Hippocampus, vol. 11, no. 5, pp. 543–550, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Malaspina, J. Harkavy-Friedman, C. Corcoran et al., “Resting neural activity distinguishes subgroups of schizophrenia patients,” Biological Psychiatry, vol. 56, no. 12, pp. 931–937, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. V. Molina, J. Sanz, F. Sarramea, C. Benito, and T. Palomo, “Prefrontal atrophy in first episodes of schizophrenia associated with limbic metabolic hyperactivity,” Journal of Psychiatric Research, vol. 39, no. 2, pp. 117–127, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. J. R. Tregellas, J. Smucny, J. G. Harris et al., “Intrinsic hippocampal activity as a biomarker for cognition and symptoms in schizophrenia,” The American Journal of Psychiatry, vol. 171, no. 5, pp. 549–556, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Talati, S. Rane, J. Skinner, J. Gore, and S. Heckers, “Increased hippocampal blood volume and normal blood flow in schizophrenia,” Psychiatry Research: Neuroimaging, vol. 232, no. 3, pp. 219–225, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. S. A. Schobel, N. H. Chaudhury, U. A. Khan et al., “Imaging patients with psychosis and a mouse model establishes a spreading pattern of hippocampal dysfunction and implicates glutamate as a driver,” Neuron, vol. 78, no. 1, pp. 81–93, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. W. Li, S. Ghose, K. Gleason et al., “Synaptic proteins in the hippocampus indicative of increased neuronal activity in CA3 in schizophrenia,” The American Journal of Psychiatry, vol. 172, no. 4, pp. 373–382, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. C. A. Tamminga, S. Southcott, C. Sacco, A. D. Wagner, and S. Ghose, “Glutamate dysfunction in hippocampus: relevance of dentate gyrus and CA3 signaling,” Schizophrenia Bulletin, vol. 38, no. 5, pp. 927–935, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. G. W. Mathern, J. K. Pretorius, D. Mendoza et al., “Increased hippocampal AMPA and NMDA receptor subunit immunoreactivity in temporal lobe epilepsy patients,” Journal of Neuropathology & Experimental Neurology, vol. 57, no. 6, pp. 615–634, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. C. A. Tamminga, A. D. Stan, and A. D. Wagner, “The hippocampal formation in schizophrenia,” The American Journal of Psychiatry, vol. 167, no. 10, pp. 1178–1193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. G. W. Mathern, J. K. Pretorius, J. P. Leite et al., “Hippocampal AMPA and NMDA mRNA levels and subunit immunoreactivity in human temporal lobe epilepsy patients and a rodent model of chronic mesial limbic epilepsy,” Epilepsy Research, vol. 32, no. 1-2, pp. 154–171, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. K. D. Murray, P. J. Isackson, T. A. Eskin et al., “Altered mRNA expression for brain-derived neurotrophic factor and type II calcium/calmodulin-dependent protein kinase in the hippocampus of patients with intractable temporal lobe epilepsy,” Journal of Comparative Neurology, vol. 418, no. 4, pp. 411–422, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Koyama and Y. Ikegaya, “Mossy fiber sprouting as a potential therapeutic target for epilepsy,” Current Neurovascular Research, vol. 1, no. 1, pp. 3–10, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Koyama, “Dentate circuitry as a model to study epileptogenesis,” Biological & Pharmaceutical Bulletin, vol. 39, no. 6, pp. 891–896, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. Q. Zhong, B.-X. Ren, and F.-R. Tang, “Neurogenesis in the hippocampus of patients with temporal lobe epilepsy,” Current Neurology and Neuroscience Reports, vol. 16, no. 2, p. 20, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. O. H. Del Brutto, J. Engel, D. S. Eliashiv, and H. H. García, “Update on cysticercosis epileptogenesis: the role of the hippocampus,” Current Neurology and Neuroscience Reports, vol. 16, no. 1, pp. 1–7, 2016. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Sierra, O. Gröhn, and A. Pitkänen, “Imaging microstructural damage and plasticity in the hippocampus during epileptogenesis,” Neuroscience, vol. 309, pp. 162–172, 2015. View at Publisher · View at Google Scholar · View at Scopus
  50. X.-B. Liu, L. K. Low, E. G. Jones, and H.-J. Cheng, “Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus,” The Journal of Neuroscience, vol. 25, no. 40, pp. 9124–9134, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Bagri, H.-J. Cheng, A. Yaron, S. J. Pleasure, and M. Tessier-Lavigne, “Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family,” Cell, vol. 113, no. 3, pp. 285–299, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Römer, J. Krebs, R. W. Overall et al., “Adult hippocampal neurogenesis and plasticity in the infrapyramidal bundle of the mossy fiber projection: I. co-regulation by activity,” Frontiers in Neuroscience, vol. 5, article 107, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Cronin and F. E. Dudek, “Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats,” Brain Research, vol. 474, no. 1, pp. 181–184, 1988. View at Publisher · View at Google Scholar · View at Scopus
  54. L. E. A. M. Mello, E. A. Cavalheiro, A. M. Tan et al., “Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting,” Epilepsia, vol. 34, no. 6, pp. 985–995, 1993. View at Publisher · View at Google Scholar · View at Scopus
  55. M. M. Okazaki, D. A. Evenson, and J. Victor Nadler, “Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin,” Journal of Comparative Neurology, vol. 352, no. 4, pp. 515–534, 1995. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Sutula, P. Zhang, M. Lynch, U. Sayin, G. Golarai, and R. Rod, “Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats,” Journal of Comparative Neurology, vol. 390, no. 4, pp. 578–594, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. P. S. Buckmaster, “Mossy Fiber Sprouting in the Dentate Gyrus,” in Jasper’s Basic Mechanisms of the Epilepsies, pp. 416–431, 2012. View at Google Scholar
  58. T. Sutula, G. Cascino, J. Cavazos, I. Parada, and L. Ramirez, “Mossy fiber synaptic reorganization in the epileptic human temporal lobe,” Annals of Neurology, vol. 26, no. 3, pp. 321–330, 1989. View at Publisher · View at Google Scholar · View at Scopus
  59. C. R. Houser, J. E. Miyashiro, B. E. Swartz, G. O. Walsh, J. R. Rich, and A. V. Delgado-Escueta, “Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy,” The Journal of Neuroscience, vol. 10, no. 1, pp. 267–282, 1990. View at Google Scholar · View at Scopus
  60. M. Isokawa, M. F. Levesque, T. L. Babb, and J. Engel Jr., “Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy,” The Journal of Neuroscience, vol. 13, no. 4, pp. 1511–1522, 1993. View at Google Scholar · View at Scopus
  61. B. El Bahh, V. Lespinet, D. Lurton, M. Coussemacq, G. Le Gal La Salle, and A. Rougier, “Correlations between granule cell dispersion, mossy fiber sprouting, and hippocampal cell loss in temporal lobe epilepsy,” Epilepsia, vol. 40, no. 10, pp. 1393–1401, 1999. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Nakahara, S. Miyake, K. Tajinda, and H. Ito, “Mossy fiber mis-pathfinding and semaphorin reduction in the hippocampus of α-CaMKII hKO mice,” Neuroscience Letters, vol. 598, pp. 47–51, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Yamasaki, M. Maekawa, K. Kobayashi et al., “Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders.,” Molecular Brain, vol. 1, p. 6, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Hattori, H. Hagihara, K. Ohira et al., “In vivo evaluation of cellular activity in αCaMKII heterozygous knockout mice using manganese-enhanced magnetic resonance imaging (MEMRI),” Frontiers in Integrative Neuroscience, vol. 7, article 76, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. S. A. Schobel, N. M. Lewandowski, C. M. Corcoran et al., “Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders,” Archives of General Psychiatry, vol. 66, no. 9, pp. 938–946, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Talati, S. Rane, S. Kose et al., “Increased hippocampal CA1 cerebral blood volume in schizophrenia,” NeuroImage: Clinical, vol. 5, pp. 359–364, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. M. A. Yassa, A. T. Mattfeld, S. M. Stark, and C. E. L. Stark, “Age-related memory deficits linked to circuit-specific disruptions in the hippocampus,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 108, no. 21, pp. 8873–8878, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. R. L. Faulkner, M.-H. Jang, X.-B. Liu et al., “Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 105, no. 37, pp. 14157–14162, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. Y. Le Strat, N. Ramoz, and P. Gorwood, “The role of genes involved in neuroplasticity and neurogenesis in the observation of a gene-environment interaction (GxE) in schizophrenia,” Current Molecular Medicine, vol. 9, no. 4, pp. 506–518, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. I. Corradini, C. Verderio, M. Sala, M. C. Wilson, and M. Matteoli, “SNAP-25 in neuropsychiatric disorders,” Annals of the New York Academy of Sciences, vol. 1152, pp. 93–99, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. J. U. Johansson, J. Ericsson, J. Janson et al., “An ancient duplication of exon 5 in the Snap25 gene is required for complex neuronal development/function,” PLoS Genetics, vol. 4, no. 11, Article ID e1000278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. S. M. Purcell, J. L. Moran, M. Fromer et al., “A polygenic burden of rare disruptive mutations in schizophrenia,” Nature, vol. 506, no. 7487, pp. 185–190, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. H. Le-Niculescu, S. D. Patel, M. Bhat et al., “Convergent functional genomics of genome-wide association data for bipolar disorder: comprehensive identification of candidate genes, pathways and mechanisms,” American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, vol. 150, no. 2, pp. 155–181, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. N. M. Walton, Y. Zhou, J. H. Kogan et al., “Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients,” Translational Psychiatry, vol. 2, p. e135, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. K. Karádi, J. Janszky, C. Gyimesi et al., “Correlation between calbindin expression in granule cells of the resected hippocampal dentate gyrus and verbal memory in temporal lobe epilepsy,” Epilepsy & Behavior, vol. 25, no. 1, pp. 110–119, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Dar, M. Glenda, W. Jun-Feng et al., “Increased hippocampal supragranular Timm staining in subjects with bipolar disorder,” NeuroReport, vol. 11, no. 17, pp. 3775–3778, 2000. View at Publisher · View at Google Scholar · View at Scopus
  77. R. Koyama, M. K. Yamada, S. Fujisawa, R. Katoh-Semba, N. Matsuki, and Y. Ikegaya, “Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus,” The Journal of Neuroscience, vol. 24, no. 33, pp. 7215–7224, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. C. Isgor, C. Pare, B. McDole, P. Coombs, and K. Guthrie, “Expansion of the dentate mossy fiber-CA3 projection in the brain-derived neurotrophic factor-enriched mouse hippocampus,” Neuroscience, vol. 288, pp. 10–23, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. M. R. Lyons and A. E. West, “Mechanisms of specificity in neuronal activity-regulated gene transcription,” Progress in Neurobiology, vol. 94, no. 3, pp. 259–295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. G. Dallérac, C. Rampon, and V. Doyère, “NCAM function in the adult brain: lessons from mimetic peptides and therapeutic potential,” Neurochemical Research, vol. 38, no. 6, pp. 1163–1173, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. R. Koyama, M. K. Yamada, N. Nishiyama, N. Matsuki, and Y. Ikegaya, “Developmental switch in axon guidance modes of hippocampal mossy fibers in vitro,” Developmental Biology, vol. 267, no. 1, pp. 29–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Seki and U. Rutishauser, “Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus,” The Journal of Neuroscience, vol. 18, no. 10, pp. 3757–3766, 1998. View at Google Scholar · View at Scopus
  83. Z. He and M. Tessier-Lavigne, “Neuropilin is a receptor for the axonal chemorepellent Semaphorin III,” Cell, vol. 90, no. 4, pp. 739–751, 1997. View at Publisher · View at Google Scholar · View at Scopus
  84. C. A. Altar, L. W. Jurata, V. Charles et al., “Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts,” Biological Psychiatry, vol. 58, no. 2, pp. 85–96, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. S. K. Goldsmith and J. N. Joyce, “Alterations in hippocampal mossy fiber pathway in Schizophrenia and Alzheimer's disease,” Biological Psychiatry, vol. 37, no. 2, pp. 122–126, 1995. View at Publisher · View at Google Scholar · View at Scopus
  86. K. J. Lee, B. N. Queenan, A. M. Rozeboom et al., “Mossy fiber-CA3 synapses mediate homeostatic plasticity in mature hippocampal neurons,” Neuron, vol. 77, no. 1, pp. 99–114, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. R. Shin, K. Kobayashi, H. Hagihara et al., “The immature dentate gyrus represents a shared phenotype of mouse models of epilepsy and psychiatric disease,” Bipolar Disorder, vol. 15, no. 4, pp. 405–421, 2013. View at Publisher · View at Google Scholar · View at Scopus
  88. G. Curia, D. Longo, G. Biagini, R. S. G. Jones, and M. Avoli, “The pilocarpine model of temporal lobe epilepsy,” Journal of Neuroscience Methods, vol. 172, no. 2, pp. 143–157, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. P. J. Isackson, M. M. Huntsman, K. D. Murray, and C. M. Gall, “BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF,” Neuron, vol. 6, no. 6, pp. 937–948, 1991. View at Publisher · View at Google Scholar · View at Scopus
  90. C. M. Gall, “Seizure-induced changes in neurotrophin expression: implications for epilepsy,” Experimental Neurology, vol. 124, no. 1, pp. 150–166, 1993. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Elmér, Z. Kokaia, M. Kokaia, J. Carnahan, H. Nawa, and O. Lindvall, “Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures,” Neuroscience, vol. 83, no. 2, pp. 351–362, 1998. View at Publisher · View at Google Scholar · View at Scopus
  92. H. Nawa, J. Carnahan, and C. Gall, “BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels,” European Journal of Neuroscience, vol. 7, no. 7, pp. 1527–1535, 1995. View at Publisher · View at Google Scholar · View at Scopus
  93. M. Mikkonen, H. Soininen, R. Kälviäinen et al., “Remodeling of neuronal circuitries in human temporal lobe epilepsy: increased expression of highly polysialylated neural cell adhesion molecule in the hippocampus and the entorhinal cortex,” Annals of Neurology, vol. 44, no. 6, pp. 923–934, 1998. View at Publisher · View at Google Scholar · View at Scopus
  94. E. A. Proper, A. B. Oestreicher, G. H. Jansen et al., “Immunohistochemical characterization of mossy fibre sprouting in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy,” Brain, vol. 123, no. 1, pp. 19–30, 2000. View at Publisher · View at Google Scholar
  95. W. Shan, M. Yoshida, X.-R. Wu, G. W. Huntley, and D. R. Colman, “Neural (N-) cadherin, a synaptic adhesion molecule, is induced in hippocampal mossy fiber axonal sprouts by seizure,” Journal of Neuroscience Research, vol. 69, no. 3, pp. 292–304, 2002. View at Publisher · View at Google Scholar · View at Scopus