Correlation between calbindin expression in granule cells of the resected hippocampal dentate gyrus and verbal memory in temporal lobe epilepsy

Epilepsy and Behavior

Volumn 25, Issue 1, 2012, Pages 110-119

  Karádi, Kázmér ^a   Janszky, József ^a,b   Gyimesi, Csilla ^a,b   Horváth, Zsolt ^a   Lucza, Tivadar ^a   Dóczi, Tamás ^a,b   Kállai, János ^a   Ábrahám, Hajnalka ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Calcium binding protein; Cortical malformation; Hippocampal sclerosis; Learning; Temporal lobe epilepsy; Tumor

Indexed keywords

CALBINDIN;

ADOLESCENT; ADULT; ARTICLE; AUDITORY VERBAL LEARNING TEST; CLINICAL ARTICLE; CLINICAL ASSESSMENT TOOL; DENTATE GYRUS; FEMALE; GRANULE CELL; HIPPOCAMPAL SCLEROSIS; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MALE; MEMORY; NEUROPSYCHOLOGY; PROTEIN EXPRESSION; TEMPORAL LOBE EPILEPSY; VERBAL MEMORY; VISUOSPATIAL MEMORY;

ACOUSTIC STIMULATION; ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; DENTATE GYRUS; EPILEPSY, TEMPORAL LOBE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MEMORY DISORDERS; MIDDLE AGED; NEURONS; NEUROPSYCHOLOGICAL TESTS; PHOSPHOPYRUVATE HYDRATASE; REGRESSION ANALYSIS; SYNAPTOPHYSIN; VERBAL LEARNING; YOUNG ADULT;

EID: 84866280452     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2012.06.007     Document Type: Article

References (87)

1. Lehericy S., Semah F., Hasboun D., et al. Temporal lobe epilepsy with varying severity: MRI study of 222 patients. Neuroradiology 1997, 39:788-796.
2. Howe K.L., Dimitri D., Heyn C., Kiehl T.R., Mikulis D., Valiante T. Histologically confirmed hippocampal structural features revealed by 3T MR imaging: potential to increase diagnostic specificity of mesial temporal sclerosis. Am J Neuroradiol 2010, 31:1682-1689.
3. Tassi L., Meroni A., Deleo F., et al. Temporal lobe epilepsy: neuropathological and clinical correlations in 243 surgically treated patients. Epileptic Disord 2009, 11:281-292.
4. Sommer W. Die Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Arch Psychiatr Nervenkr 1880, 308:631-675.
5. Dam A.M. Epilepsy and neuron loss in the hippocampus. Epilepsia 1980, 21:617-629.
6. Babb T.L., Brown W.J., Pretorius J., Davenport C., Lieb J.P., Crandall P.H. Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia 1984, 25:729-740.
7. Blümcke I., Suter B., Behle K., et al. Loss of hilar mossy cells in Ammon's horn sclerosis. Epilepsia Suppl 2000, 6:S174-S180.
8. Cronin J., Dudek F.E. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 1988, 474:181-184.
9. Represa A., Le Gall La Salle G., Ben-Ari Y. Hippocampal plasticity in the kindling model of epilepsy in rats. Neurosci Lett 1989, 99:345-350.
10. de Lanerolle N.C., Kim J.H., Robbins R.J., Spencer D.D. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 1989, 495:387-395.
11. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 1989, 26:321-330.
12. Davenport C.J., Brown W.J., Babb T.L. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp Neurol 1990, 109:180-190.
13. Houser C.R., Miyashiro J.E., Swartz B.E., Walsh G.O., Rich J.R., Delgado-Escueta A.V. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 1990, 10:267-282.
14. Maglóczky Z., Wittner L., Borhegyi Z., et al. Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 2000, 96:7-25.
15. Wittner L., Eross L., Szabó Z., et al. Synaptic reorganization of calbindin-positive neurons in the human hippocampal CA1 region in temporal lobe epilepsy. Neuroscience 2002, 115:961-978.
16. Kim J.H., Guimaraes P.O., Shen M.Y., Masukawa L.M., Spencer D.D. Hippocampal neuronal density in temporal lobe epilepsy with and without gliomas. Acta Neuropathol 1990, 80:41-45.
17. Blümcke I., Beck H., Lie A.A., Wiestler O.D. Molecular pathology of human mesial temporal lobe epilepsy. Epilepsy Res 1999, 36:205-223.
18. de Lanerolle N.C., Kim J.H., Williamson A., et al. A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 2003, 44:677-687.
19. Abrahám H., Richter Z., Gyimesi C., et al. 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 Res 2011, 1399:66-78.
20. Awad I.A., Rosenfeld J., Ahl J., Hahn J.F., Lüders H. Intractable epilepsy and structural lesions of the brain: mapping, resection strategies, and seizure outcome. Epilepsia 1991, 32:179-186.
21. Berger M.S., Ghatan S., Haglund M.M., Dobbins J., Ojemann G.A. Low-grade gliomas associated with intractable epilepsy: seizure outcome utilizing electrocorticography during tumor resection. J Neurosurg 1993, 79:62-69.
22. Cascino G.D., Jack C.R., Parisi J.E., et al. Operative strategy in patients with MRI-identified dual pathology and temporal lobe epilepsy. Epilepsy Res 1993, 14:175-182.
23. Mathern G.W., Babb T.L., Pretorius J.K., Melendez M., Lévesque M.F. The pathophysiologic relationships between lesion pathology, intracranial ictal EEG onsets, and hippocampal neuron losses in temporal lobe epilepsy. Epilepsy Res 1995, 21:133-147.
24. Maglóczky Z.S., Halász P., Vajda J., Czirják S., Freund T.F. Loss of calbindin-D28K immunoreactivity from dentate granule cells in human temporal lobe epilepsy. Neuroscience 1997, 76:377-385.
25. Nagerl U.V., Mody I. Calcium-dependent inactivation of high-threshold calcium currents in human dentate gyrus granule cells. J Physiol 1998, 509:39-45.
26. Nägerl U.V., Mody I., Jeub M., Lie A.A., Elger C.E., Beck H. Surviving granule cells of the sclerotic human hippocampus have reduced Ca(2+) influx because of a loss of calbindin-D(28k) in temporal lobe epilepsy. J Neurosci 2000, 20:1831-1836.
27. Bouilleret V., Schwaller B., Schurmans S., Celio M.R., Fritschy J.M. Neurodegenerative and morphogenic changes in a mouse model of temporal lobe epilepsy do not depend on the expression of the calcium-binding proteins parvalbumin, calbindin, or calretinin. Neuroscience 2000, 97:47-58.
28. Gary D.S., Sooy K., Chan S.L., Christakos S., Mattson M.P. Concentration- and cell type-specific effects of calbindin D28k on vulnerability of hippocampal neurons to seizure-induced injury. Brain Res Mol Brain Res 2000, 75:89-95.
29. Molinari S., Battini R., Ferrari S., et al. Deficits in memory and hippocampal long-term potentiation in mice with reduced calbindin D28K expression. Proc Natl Acad Sci U S A 1996, 93:8028-8033.
30. Jouvenveau A., Potier B., Poindessous-Jazat F., et al. Decrease in calbindin content significantly alters LTP but not NMDA receptor and calciun channel properties. Neuropharmacology 2002, 42:444-458.
31. Nadel L., Willner J. Some implications of postnatal maturation of hippocampus. The hippocampus 1989, 17-31. New Vistas, New York. V. Chan-Palay, C. Köhler, A.R. Liss (Eds.).
32. Ábrahám H., Orsi G., Seress L. Ontogeny of cocaine- and amphetamine-regulated transcript (CART) peptide and calbindin immunoreactivity in granule cells of the dentate gyrus in the rat. Int J Dev Neurosci 2007, 25:265-274.
33. Overman W.H., Pate B.J., Moore K., Peuster A. Ontogeny of place learning in children as measured in the radial arm maze, Morris search task, and open field task. Behav Neurosci 1996, 110:1205-1228.
34. Ábrahám H., Veszprémi B., Kravják A., Kovács K., Gömöri E., Seress L. Ontogeny of calbindin immunoreactivity in the human hippocampal formation with a special emphasis on granule cells of the dentate gyrus. Int J Dev Neurosci 2009, 27:115-127.
35. Collier T.J., Routtenberg A. Selective impairment of declarative memory following stimulation of dentate gyrus granule cells: a naloxone-sensitive effect. Brain Res 1984, 310:384-387.
36. Cave C.B., Squire L.R. Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus. Hippocampus 1991, 1:329-340.
37. Mameniskiene R., Jatuzis D., Kaubrys G., Budry V. The decay of memory between delayed and long-term recall in patients with temporal lobe epilepsy. Epilepsy Behav 2006, 8:278-288.
38. Marques C.M., Caboclo L.O.S.F., da Silva T.I., et al. Cognitive decline in temporal epilepsy due to unilateral hippocampal sclerosis. Epilepsy Behav 2007, 10:477-485.
39. Herfurth K., Kasper B., Schwarz M., Stefan H., Pauli E. Autobiographical memory in temporal lobe epilepsy: role of hippocampal and temporal lateral structures. Epilepsy Behav 2010, 19:365-371.
40. Tudesco Ide S., Vaz L.J., Mantoan M.A., et al. Assessment of working memory in patients with mesial temporal lobe epilepsy associated with unilateral hippocampal sclerosis. Epilepsy Behav 2010, 18:223-228.
41. Helmstaedter C., Wietzke J., Lutz M.T. Unique and shared validity of the "Wechsler logical memory test", the "California verbal learning test", and the "verbal learning and memory test" in patients with epilepsy. Epilepsy Res 2009, 87:203-212.
42. Alessio A., Damasceno B.P., Camargo C.H.P., Kobayashi E., Guerreiro C.A.M., Cendes F. Differences in memory performance and other clinical characteristics in patients with mesial temporal lobe epilepsy with and without hippocampal atrophy. Epilepsy Behav 2004, 5:22-27.
43. 1H MRS and memory before and after surgery in mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 2004, 45:632-640.
44. Sass K.J., Spencer D.D., Kim J.H., Westerveld M., Novelly R.A., Lencz T. Verbal memory impairment correlates with hippocampal pyramidal cell density. Neurology 1990, 40:1694-1697.
45. Sass K.J., Sass A., Westerveld M., et al. Specificity in the correlation of verbal memory and hippocampal neuron loss: dissociation of memory, language, and verbal intellectual ability. J Clin Exp Neuropsychol 1992, 14:662-672.
46. Sass K.J., Westerveld M., Buchanan C.P., Spencer S.S., Kim J.H., Spencer D.D. Degree of hippocampal neuron loss determines severity of verbal memory decrease after left anteromesiotemporal lobectomy. Epilepsia 1994, 35:1179-1186.
47. Sass K.J., Buchanan C.P., Kraemer S., Westerveld M., Kim J.H., Spencer D.D. Verbal memory impairment resulting from hippocampal neuron loss among epileptic patients with structural lesions. Neurology 1995, 45:2154-2158.
48. Rausch R., Babb T.L. Hippocampal neuron loss and memory scores before and after temporal lobe surgery for epilepsy. Arch Neurol 1993, 50:812-817.
49. Pauli E., Hildebrandt M., Romstöck J., Stefan H., Blümcke I. Deficient memory acquisition in temporal lobe epilepsy is predicted by hippocampal granule cell loss. Neurology 2006, 67:1383-1389.
50. Coras R., Siebzehnrubl F.A., Pauli E., et al. Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans. Brain 2010, 133:3359-3372.
51. Lezak M.D., Howieson D.B., Loring D.W. Neuropsychological assessment 2004, Oxford University Press, Oxford.
52. Hodges J.R. Cognitive assessment for clinicians 1996, Oxford Uviversity Press, Oxford.
53. Mitrushina M.N., Boone K.B., D'Elia L.F. Handbook of normative data for neuropsychological assessment 1999, Oxford University Press, Oxford.
54. Lilliwhite L.M., Saling M.M., Briellman R.S., Weintrob D.L., Pell G.S., Jackson G.D. Differential contributions of the hippocampus and rhinal cortices to verbal memory in epilepsy. Epilepsy Behav 2007, 10:553-559.
55. Abrahám H., Tornóczky T., Kosztolányi G., Seress L. Cell formation in the cortical layers of the developing human cerebellum. Int J Dev Neurosci 2001, 19:53-62.
56. Seress L., Abrahám H., Tornóczky T., Kosztolányi G. Cell formation in the human hippocampal formation from mid-gestation to the late postnatal period. Neuroscience 2001, 105:831-843.
57. Sloviter R.S., Kudrimoti H.S., Laxer K.D., et al. "Tectonic" hippocampal malformations in patients with temporal lobe epilepsy. Epilepsy Res 2004, 59:123-153.
58. Wyler A.R., Dohan F.C., Schweitzer J.B., Berry A.D. A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy. J Epilepsy 1992, 5:220-225.
59. Thom M., Liagkouras I., Elliot K.J., et al. Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 2010, 51:1801-1808.
60. Blümcke I., Pauli E., Clusmann H., et al. A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 2007, 113:235-244.
61. Blümcke I., Kistner I., Clusmann H., et al. Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathol 2009, 117:535-544.
62. Blümcke I., Thom M., Aronica E., et al. The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 2011, 52:158-174.
63. Elger C.E., Grunwald T., Lehnertz K., et al. Human temporal lobe potentials in verbal learning and memory processes. Neuropsychologia 1997, 35:657-667.
64. Babiloni C., Vecchio F., Mirabella G., et al. Activity of hippocampal, amygdala, and neocortex during the Rey auditory verbal learning test: an event-related potential study in epileptic patients. Clin Neurophysiol 2010, 121:1351-1357.
65. Hopkins R.O., Waldram K., Kesner R.P. Sequences assessed by declarative and procedural tests of memory in amnesic patients with hippocampal damage. Neuropsychologia 2004, 42:1877-1886.
66. Carter D.S., Harrison A.J., Falenski K.W., Blair R.E., DeLorenzo R.J. Long-term decrease in calbindin-D28K expression in the hippocampus of epileptic rats following pilocarpine-induced status epilepticus. Epilepsy Res 2008, 79:213-223.
67. Magloczky Z., Freund T.F. Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience 1993, 56:317-335.
68. Martinian L., Catarino C.B., Thompson P., Sisodiya S.M., Thom M. Calbindin D28K expression in relation to granule cell dispersion, mossy fibre sprouting and memory impairment in hippocampal sclerosis: a surgical and post mortem series. Epilepsy Res 2012, 98:14-24.
69. Lledo P.M., Somasundaram B., Morton A.J., Emson P.C., Mason W.T. Stable transfection of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeostasis. Neuron 1992, 9:943-954.
70. Palop J.J., Jones B., Kekonius L., et al. Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci U S A 2003, 100:9572-9577.
71. Odero G.L., Oikawa K., Glazner K.A., et al. Evidence for the involvement of calbindin D28k in the presenilin 1 model of Alzheimer's disease. Neuroscience 2010, 169:532-543.
72. Real M.A., Simón M.P., Heredia R., de Diego Y., Guirado S. Phenotypic changes in calbindin D28K immunoreactivity in the hippocampus of Fmr1 knockout mice. J Comp Neurol 2011, 519:2622-2636.
73. Toepper M., Markowitsch H.J., Gebhardt H., et al. Hippocampal involvement in working memory encoding of changing locations: an fMRI study. Brain Res 2010, 1354:91-99.
74. Kneebone A.C., Lee G.P., Wade L.T., Loring D.W. Rey Complex Figure: figural and spatial memory before and after temporal lobectomy for intractable epilepsy. J Int Neuropsychol Soc 2007, 13:664-671.
75. McConley R., Martin R., Palmer C.A., Kuzniecky R., Knowlton R., Faught E. Rey Osterrieth complex figure test spatial and figural scoring: relations to seizure focus and hippocampal pathology in patients with temporal lobe epilepsy. Epilepsy Behav 2008, 13:174-177.
76. Waber D.P., Holmes J.M. Assessing children's memory productions of the Rey-Osterrieth Complex Figure. J Clin Exp Neuropsychol 1986, 8:563-580.
77. Barr W.B. Examining the right temporal lobe's role in nonverbal memory. Brain Cogn 1997, 35:26-41.
78. Baxendale S.A., Thompson P.J., Van Paesschen W. A test of spatial memory and its clinical utility in the pre-surgical investigation of temporal lobe epilepsy patients. Neuropsychologia 1998, 36:591-602.
79. Raspall T., Donate M., Boget T., et al. Neuropsychological tests with lateralizing value in patients with temporal lobe epilepsy: reconsidering material-specific theory. Seizure 2005, 14:569-576.
80. Maguire E.A., Woollett K., Spiers H.J. London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 2006, 16:1091-1101.
81. Maguire E.A., Burke T., Phillips J., Staunton H. Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia 1996, 34:993-1001.
82. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S., Frith C.D., O'Keefe J. Knowing where and getting there: a human navigation network. Science 1998, 280:921-924.
83. Ghaem O., Mellet E., Crivello F., et al. Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport 1997, 8:739-744.
84. Grön G., Wunderlich A.P., Spitzer M., Tomczak R., Riepe M.W. Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat Neurosci 2000, 3:404-408.
85. Spiers H.J., Maguire E.A. Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 2006, 31:1826-1840.
86. Maguire E.A., Frith C.D. Lateral asymmetry in the hippocampal response to the remoteness of autobiographical memories. J Neurosci 2003, 23:5302-5307.
87. Viskontas I.V., McAndrews M.P., Moscovitch M. Remote episodic memory deficits in patients with unilateral temporal lobe epilepsy and excisions. J Neurosci 2000, 20:5853-5857.