Is exposure to enriched environment beneficial for functional post-lesional recovery in temporal lobe epilepsy?

Neuroscience and Biobehavioral Reviews

Volumn 32, Issue 4, 2008, Pages 657-674

  Dhanushkodi, Anandh ^a,b   Shetty, Ashok K ^a,b  

^a DURHAM VA MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Dentate neurogenesis; Enriched environment; Epilepsy; Neuronal plasticity; Neuroprotection; Seizures

Indexed keywords

ANTIDEPRESSANT AGENT; CYTARABINE; NEUROTROPHIC FACTOR;

ALZHEIMER DISEASE; BRAIN INJURY; COGNITION; CONVALESCENCE; DEGENERATIVE DISEASE; DEPRESSION; DRUG MECHANISM; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; EPILEPTOGENESIS; HIPPOCAMPUS; HUMAN; MENTAL DEFICIENCY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEIZURE; TEMPORAL LOBE EPILEPSY;

ANIMALS; BRAIN CHEMISTRY; COGNITION; ENVIRONMENT; EPILEPSY, TEMPORAL LOBE; HUMANS; RECOVERY OF FUNCTION;

EID: 40149100452     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2007.10.004     Document Type: Review

References (218)

1. Abraham W.C., Logan B., Greenwood J.M., and Dragunow M. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. Journal of Neuroscience 22 (2002) 9626-9634
2. Abrous D.N., Koehl M., and Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiological Reviews 85 (2005) 523-569
3. Aimone J.B., Wiles J., and Gage F.H. Potential role for adult neurogenesis in the encoding of time in new memories. Nature Neuroscience 9 (2006) 723-727
4. Arendash G.W., Garcia M.F., Costa D.A., Cracchiolo J.R., Wefes I.M., and Potter H. Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. Neuroreport 15 (2004) 1751-1754
5. Auvergne R., Lere C., El Bahh B., Arthaud S., Lespinet V., Rougier A., and Le Gal La Salle G. Delayed kindling epileptogenesis and increased neurogenesis in adult rats housed in an enriched environment. Brain Research 954 (2002) 277-285
6. Avoli M., D'Antuono M., Louvel J., Kohling R., Biagini G., Pumain R., D'Arcangelo G., and Tancredi V. Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Progress in Neurobiology 68 (2002) 167-207
7. Bausch S.B., and McNamara J.O. Contributions of mossy fiber and CA1 pyramidal cell sprouting to dentate granule cell hyperexcitability in kainic acid-treated hippocampal slice cultures. Journal of Neurophysiology 92 (2004) 3582-3595
8. Belayev A., Saul I., Liu Y., Zhao W., Ginsberg M.D., Valdes M.A., Busto R., and Belayev L. Enriched environment delays the onset of hippocampal damage after global cerebral ischemia in rats. Brain Research 964 (2003) 121-127
9. Ben-Ari Y., Repressa A., Tremblay E., and Nitecka L. Selective and non-selective seizure related brain damage produced by kainic acid. Advances in Experimental Medicine and Biology 203 (1986) 647-657
10. Bezard E., Dovero S., Belin D., Duconger S., Jackson-Lewis V., Przedborski S., Piazza P.V., Gross C.E., and Jaber M. Enriched environment confers resistance to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. Journal of Neuroscience 23 (2003) 10999-11007
11. Biernaskie J., and Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. Journal of Neuroscience 21 (2001) 5272-5280
12. Binder D.K., and Scharfman H.E. Brain-derived neurotrophic factor. Growth Factors 22 (2004) 123-131
13. Binder D.K., Croll S.D., Gall C.M., and Scharfman H.E. BDNF and epilepsy: too much of a good thing?. Trends in Neuroscience 24 (2001) 47-53
14. Bindu B., Rekha J., and Kutty B.M. Post insult enriched housing improves the 8-arm radial maze performance but not the Morris water maze task in ventral subicular lesioned rats. Brain Research 1063 (2005) 121-131
15. Bindu B., Alladi P.A., Mansooralikhan B.M., Srikumar B.N., Raju T.R., and Kutty B.M. Short-term exposure to an enriched environment enhances dendritic branching but not brain-derived neurotrophic factor expression in the hippocampus of rats with ventral subicular lesions. Neuroscience 144 (2007) 412-423
16. Bowling S.L., Rowlett J.K., and Bardo M.T. The effect of environmental enrichment on amphetamine-stimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology 32 (1993) 885-893
17. Branchi I., Francia N., and Alleva E. Epigenetic control of neurobehavioural plasticity: the role of neurotrophins. Behavioural Pharmacology 15 (2004) 353-362
18. Branchi I., D'Andrea I., Fiore M., Di Fausto V., Aloe L., and Alleva E. Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biological Psychiatry 60 (2006) 690-696
19. Bredy T.W., Zhang T.Y., Grant R.J., Diorio J., and Meaney M.J. Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression. European Journal of Neuroscience 20 (2004) 1355-1362
20. Briones T.L., Therrien B., and Metzger B. Effects of environment on enhancing functional plasticity following cerebral ischemia. Biological Research for Nursing 1 (2000) 299-309
21. Brockington A., Lewis C., Wharton S., and Shaw P.J. Vascular endothelial growth factor and the nervous system. Neuropathology and Applied Neurobiology 30 (2004) 427-446
22. Buhl E.H., Otis T.S., and Mody I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271 (1996) 369-373
23. Carro E., Trejo J.L., Nunez A., and Torres-Aleman I. Brain repair and neuroprotection by serum insulin-like growth factor I. Molecular Neurobiology 27 (2003) 153-162
24. Cavazos J.E., Zhang P., Qazi R., and Sutula T.P. Ultrastructural features of sprouted mossy fiber synapses in kindled and kainic acid-treated rats. Journal of Comparative Neurology 458 (2003) 272-292
25. Clusmann H., Schramm J., Kral T., Helmstaedter C., Ostertun B., Fimmers R., Haun D., and Elger C.E. Prognostic factors and outcome after different types of resection for temporal lobe epilepsy. Journal of Neurosurgery 97 (2002) 1131-1141
26. Comery T.A., Harris J.B., Willems P.J., Oostra B.A., Irwin S.A., Weiler I.J., and Greenough W.T. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proceedings of National Academy of Science USA 94 (1997) 5401-5404
27. Cronin J., and Dudek F.E. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Research 474 (1988) 181-184
28. Cummins R.A., and Livesey P.J. Enrichment-isolation, cortex length and the rank order effect. Brain Research 178 (1979) 89-98
29. Del Arco A., Segovia G., Canales J.J., Garrido P., de Blas M., Garcia-Verdugo J.M., and Mora F. Environmental enrichment reduces the function of D1 dopamine receptors in the prefrontal cortex of the rat. Journal of Neural Transmission 114 (2007) 43-48
30. Devinsky O. Diagnosis and treatment of temporal lobe epilepsy. Review of Neurological Disorder 1 (2004) 2-9
31. Dhanushkodi A., Bindu B., Raju T.R., and Kutty B.M. Exposure to enriched environment improves spatial learning performances and enhances cell density but not choline acetyltransferase activity in the hippocampus of ventral subicular-lesioned rats. Behavioural Neuroscience 121 (2007) 491-500
32. Drapeau E., Mayo W., Aurousseau C., Le Moal M., Piazza P.V., and Abrous D.N. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proceedings of National Academy of Science USA 100 (2003) 14385-14390
33. Drapeau E., Montaron M.F., Aguerre S., and Abrous D.N. Learning-induced survival of new neurons depends on the cognitive status of aged rats. Journal of Neuroscience 27 (2007) 6037-6044
34. Dudek F.E., Obenaus A., Schweitzer J.S., and Wuarin J.P. Functional significance of hippocampal plasticity in epileptic brain: electrophysiological changes of the dentate granule cells associated with mossy fiber sprouting. Hippocampus 4 (1994) 259-265
35. Duffy S.N., Craddock K.J., Abel T., and Nguyen P.V. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learning and Memory 8 (2001) 26-34
36. During M.J., and Cao L. VEGF, a mediator of the effect of experience on hippocampal neurogenesis. Current Alzheimer Research 3 (2006) 29-33
37. Ehninger D., and Kempermann G. Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cerebral Cortex 13 (2003) 845-851
38. Engel Jr. J. A greater role for surgical treatment of epilepsy: why and when?. Epilepsy Currents 3 (2003) 37-40
39. Engel Jr. J., Babb T.L., and Crandall P.H. Surgical treatment of epilepsy: opportunities for research into basic mechanisms of human brain function. Acta Neurochirurgica Supplement (Wien) 46 (1989) 3-8
40. Fan Y., Liu Z., Weinstein P.R., Fike J.R., and Liu J. Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. European Journal of Neuroscience 25 (2007) 38-46
41. Farrell R., Evans S., and Corbett D. Environmental enrichment enhances recovery of function but exacerbates ischemic cell death. Neuroscience 107 (2001) 585-592
42. Faverjon S., Silveira D.C., Fu D.D., Cha B.H., Akman C., Hu Y., and Holmes G.L. Beneficial effects of enriched environment following status epilepticus in immature rats. Neurology 59 (2002) 1356-1364
43. Foster T.C., and Dumas T.C. Mechanism for increased hippocampal synaptic strength following differential experience. Journal of Neurophysiology 85 (2001) 1377-1383
44. Foster T.C., Gagne J., and Massicotte G. Mechanism of altered synaptic strength due to experience: relation to long-term potentiation. Brain Research 736 (1996) 243-250
45. French J.A., Williamson P.D., Thadani V.M., Darcey T.M., Mattson R.H., Spencer S.S., and Spencer D.D. Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Annals of Neurology 34 (1993) 774-780
46. Gage F.H. Neurogenesis in the adult brain. Journal of Neuroscience 22 (2002) 612-613
47. Galani R., Jarrard L.E., Will B.E., and Kelche C. Effects of postoperative housing conditions on functional recovery in rats with lesions of the hippocampus, subiculum, or entorhinal cortex. Neurobiology of Learning and Memory 67 (1997) 43-56
48. Gaulke L.J., Horner P.J., Fink A.J., McNamara C.L., and Hicks R.R. Environmental enrichment increases progenitor cell survival in the dentate gyrus following lateral fluid percussion injury. Brain Research Molecular Brain Research 141 (2005) 138-150
49. Ge S., Pradhan D.A., Ming G.L., and Song H. GABA sets the tempo for activity-dependent adult neurogenesis. Trends in Neuroscience 30 (2007) 1-8
50. Glass M., van Dellen A., Blakemore C., Hannan A.J., and Faull R.L. Delayed onset of Huntington's disease in mice in an enriched environment correlates with delayed loss of cannabinoid CB1 receptors. Neuroscience 123 (2004) 207-212
51. Gobbo O.L., and O'Mara S.M. Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behavioural Brain Research 152 (2004) 231-241
52. Gong C., Wang T.W., Huang H.S., and Parent J.M. Reelin regulates neuronal progenitor migration in intact and epileptic hippocampus. Journal of Neuroscience 27 (2007) 1803-1811
53. Gorter J.A., van Vliet E.A., Aronica E., and Lopes da Silva F.H. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. European Journal of Neuroscience 13 (2001) 657-669
54. Gorter J.A., Goncalves Pereira P.M., van Vliet E.A., Aronica E., Lopes da Silva F.H., and Lucassen P.J. Neuronal cell death in a rat model for mesial temporal lobe epilepsy is induced by the initial status epilepticus and not by later repeated spontaneous seizures. Epilepsia 44 (2003) 647-658
55. Gould E. How widespread is adult neurogenesis in mammals?. Nature Review Neuroscience 8 (2007) 481-488
56. Greenough W.T., and Volkmar F.R. Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Experimental Neurology 40 (1973) 491-504
57. Greenough W.T., Volkmar F.R., and Juraska J.M. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Experimental Neurology 41 (1973) 371-378
58. Hattiangady B., Rao M.S., and Shetty A.K. Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus. Neurobiology of Disease 17 (2004) 473-490
59. Hattiangady B., Rao M.S., Shetty G.A., and Shetty A.K. Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Experimental Neurology 195 (2005) 353-371
60. Hattiangady B., Rao M.S., Zaman V., and Shetty A.K. Incorporation of embryonic CA3 cell grafts into the adult hippocampus at 4-months after injury: effects of combined neurotrophic supplementation and caspase inhibition. Neuroscience 139 (2006) 1369-1383
61. Hattori S., Hashimoto R., Miyakawa T., Yamanaka H., Maeno H., Wada K., and Kunugi H. Enriched environments influence depression-related behavior in adult mice and the survival of newborn cells in their hippocampi. Behavioural Brain Research 180 (2007) 69-76
62. Hebb D.O. The effects of early experience on problem-solving at maturity. American Psychology 2 (1947) 306-307
63. Hellier J.L., Patrylo P.R., Dou P., Nett M., Rose G.M., and Dudek F.E. Assessment of inhibition and epileptiform activity in the septal dentate gyrus of freely behaving rats during the first week after kainate treatment. Journal of Neuroscience 19 (1999) 10053-10064
64. Hickmott P.W., and Ethell I.M. Dendritic plasticity in the adult neocortex. Neuroscientist 12 (2006) 16-28
65. Hockly E., Cordery P.M., Woodman B., Mahal A., van Dellen A., Blakemore C., Lewis C.M., Hannan A.J., and Bates G.P. Environmental enrichment slows disease progression in R6/2 Huntington's disease mice. Annals of Neurology 51 (2002) 235-242
66. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Research 535 (1990) 195-204
67. Huang E.J., and Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annual Review of Neuroscience 24 (2001) 677-736
68. Huang F.L., Huang K.P., and Boucheron C. Long-term enrichment enhances the cognitive behavior of the aging neurogranin null mice without affecting their hippocampal LTP. Learn and Memory 14 (2007) 512-519
69. Irvine G.I., Logan B., Eckert M., and Abraham W.C. Enriched environment exposure regulates excitability, synaptic transmission, and LTP in the dentate gyrus of freely moving rats. Hippocampus 16 (2006) 149-160
70. Jadavji N.M., Kolb B., and Metz G.A. Enriched environment improves motor function in intact and unilateral dopamine-depleted rats. Neuroscience 140 (2006) 1127-1138
71. Jakubs K., Nanobashvili A., Bonde S., Ekdahl C.T., Kokaia Z., Kokaia M., and Lindvall O. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 52 (2006) 1047-1059
72. Jankowsky J.L., Xu G., Fromholt D., Gonzales V., and Borchelt D.R. Environmental enrichment exacerbates amyloid plaque formation in a transgenic mouse model of Alzheimer disease. Journal of Neuropathology Experimental Neurology 62 (2003) 1220-1227
73. Jankowsky J.L., Melnikova T., Fadale D.J., Xu G.M., Slunt H.H., Gonzales V., Younkin L.H., Younkin S.G., Borchelt D.R., and Savonenko A.V. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. Journal of Neuroscience 25 (2005) 5217-5224
74. Jeffery K.J. LTP and spatial learning-where to next?. Hippocampus 7 (1997) 95-110
75. Jessberger S., Zhao C., Toni N., Clemenson Jr. G.D., Li Y., and Gage F.H. Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. Journal of Neuroscience 27 (2007) 9400-9407
76. Johansson B.B. Environmental influence on outcome after experiment brain infarction. Acta Neurochirurgica Supplement 66 (1996) 63-67
77. Johansson B.B. Functional outcome in rats transferred to an enriched environment 15 days after focal brain ischemia. Stroke 27 (1996) 324-326
78. Johansson B.B., and Belichenko P.V. Neuronal plasticity and dendritic spines: effect of environmental enrichment on intact and postischemic rat brain. Journal of Cerebral Blood Flow and Metabolism 22 (2002) 89-96
79. Johansson B.B., and Ohlsson A.L. Environment, social interaction, and physical activity as determinants of functional outcome after cerebral infarction in the rat. Experimental Neurology 139 (1996) 322-327
80. Jung K.H., Chu K., Kim M., Jeong S.W., Song Y.M., Lee S.T., Kim J.Y., Lee S.K., and Roh J.K. Continuous cytosine-β-d-arabinofuranoside infusion reduces ectopic granule cells in adult rat hippocampus with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. European Journal of Neuroscience 19 (2004) 3219-3226
81. Jutila L., Immonen A., Partanen K., Partanen J., Mervaala E., Ylinen A., Alafuzoff I., Paljarvi L., Karkola K., Vapalahti M., and Pitkanen A. Neurobiology of epileptogenesis in the temporal lobe. Advances and Technical Standards in Neurosurgery 27 (2002) 5-22
82. Kaplan M.S., and Hinds J.W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197 (1977) 1092-1094
83. Kee N., Teixeira C.M., Wang A.H., and Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nature Neuroscience 10 (2007) 355-362
84. Kelche C., Dalrymple-Alford J., and Will B. Effects of postoperative environment on recovery of function after fimbria-fornix transaction in the rat. Physiology and Behaviour 40 (1987) 731-736
85. Kempermann G., Kuhn H.G., and Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386 (1997) 493-495
86. Kempermann G., Gast D., and Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Annals of Neurology 52 (2002) 135-143
87. Kempermann G., Wiskott L., and Gage F.H. Functional significance of adult neurogenesis. Current Opinion in Neurobiology 14 (2004) 186-191
88. Kobayashi S., Ohashi Y., and Ando S. Effects of enriched environments with different durations and starting times on learning capacity during aging in rats assessed by a refined procedure of the Hebb-Williams maze task. Journal of Neuroscience Research 70 (2002) 340-346
89. Koh S., Chung H., Xia H., Mahadevia A., and Song Y. Environmental enrichment reverses the impaired exploratory behavior and altered gene expression induced by early-life seizures. Journal of Child Neurology 20 (2005) 796-802
90. Koh S., Magid R., Chung H., Stine C.D., and Wilson D.N. Depressive behavior and selective downregulation of serotonin receptor expression after early-life seizures: reversal by environmental enrichment. Epilepsy and Behaviour 10 (2007) 26-31
91. Komitova M., Perfilieva E., Mattsson B., Eriksson P.S., and Johansson B.B. Effects of cortical ischemia and postischemic environmental enrichment on hippocampal cell genesis and differentiation in the adult rat. Journal of Cerebral Blood Flow and Metabolism 22 (2002) 852-860
92. Komitova M., Mattsson B., Johansson B.B., and Eriksson P.S. Enriched environment increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of stroke-lesioned adult rats. Stroke 36 (2005) 1278-1282
93. Komitova M., Zhao L.R., Gido G., Johansson B.B., and Eriksson P. Postischemic exercise attenuates whereas enriched environment has certain enhancing effects on lesion-induced subventricular zone activation in the adult rat. European Journal of Neuroscience 21 (2005) 2397-2405
94. Komitova M., Perfilieva E., Mattsson B., Eriksson P.S., and Johansson B.B. Enriched environment after focal cortical ischemia enhances the generation of astroglia and NG2 positive polydendrocytes in adult rat neocortex. Experimental Neurology 199 (2006) 113-121
95. Koyama R., and Ikegaya Y. Mossy fiber sprouting as a potential therapeutic target for epilepsy. Current Neurovascular Research 1 (2004) 3-10
96. Koyama R., and Ikegaya Y. To BDNF or not to BDNF: that is the epileptic hippocampus. Neuroscientists 11 (2005) 282-287
97. Koyama R., Yamada M.K., Fujisawa S., Katoh-Semba R., Matsuki N., and Ikegaya Y. Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus. Journal of Neuroscience 24 (2004) 7215-7224
98. Lazic S.E., Grote H.E., Blakemore C., Hannan A.J., van Dellen A., Phillips W., and Barker R.A. Neurogenesis in the R6/1 transgenic mouse model of Huntington's disease: effects of environmental enrichment. European Journal of Neuroscience 23 (2006) 1829-1838
99. Leuner B., Gould E., and Shors T.J. Is there a link between adult neurogenesis and learning?. Hippocampus 16 (2006) 216-224
100. Levi O., and Michaelson D.M. Environmental enrichment stimulates neurogenesis in apolipoprotein E3 and neuronal apoptosis in apolipoprotein E4 transgenic mice. Journal of Neurochemistry 100 (2007) 202-210
101. Lewis D.V. Losing neurons: selective vulnerability and mesial temporal sclerosis. Epilepsia 46 Suppl. 7 (2005) 39-44
102. Litt B., Esteller R., Echauz J., D'Alessandro M., Shor R., Henry T., Pennell P., Epstein C., Bakay R., Dichter M., and Vachtsevanos G. Epileptic seizures may begin hours in advance of clinical onset: a report of five patients. Neuron 30 (2001) 51-64
103. Lynch M., and Sutula T. Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. Journal of Neurophysiology 83 (2000) 693-704
104. Martin R., Sawrie S., Gilliam F., Mackey M., Faught E., Knowlton R., and Kuzniekcy R. Determining reliable cognitive change after epilepsy surgery: development of reliable change indices and standardized regression-based change norms for the WMS-III and WAIS-III. Epilepsia 43 (2002) 1551-1558
105. Masukawa L.M., Higashima M., Kim J.H., and Spencer D.D. Epileptiform discharges evoked in hippocampal brain slices from epileptic patients. Brain Research 493 (1989) 168-174
106. Masukawa L.M., Uruno K., Sperling M., O'Connor M.J., and Burdette L.J. The functional relationship between antidromically evoked field responses of the dentate gyrus and mossy fiber reorganization in temporal lobe epileptic patients. Brain Research 579 (1992) 119-127
107. Mathern G.W., Cifuentes F., Leite J.P., Pretorius J.K., and Babb T.L. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalography and Clinical Neurophysiology 87 (1993) 326-339
108. Mathern G.W., Babb T.L., Pretorius J.K., and Leite J.P. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. Journal of Neuroscience 15 (1995) 3990-4004
109. Mathern G.W., Leite J.P., Pretorius J.K., Quinn B., Peacock W.J., and Babb T.L. Severe seizures in young children are associated with hippocampal neuron losses and aberrant mossy fiber sprouting during fascia dentata postnatal development. Epilepsy Research Supplement 12 (1996) 33-43
110. Mayr B., and Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nature Reviews Molecular Cell Biology 2 (2001) 599-609
111. Mayr B.M., Canettieri G., and Montminy M.R. Distinct effects of cAMP and mitogenic signals on CREB-binding protein recruitment impart specificity to target gene activation via CREB. Proceedings of National Academy of Science USA 98 (2001) 10936-10941
112. Mayr B.M., Guzman E., and Montminy M. Glutamine rich and basic region/leucine zipper (bZIP) domains stabilize cAMP-response element-binding protein (CREB) binding to chromatin. Journal of Biological Chemistry 280 (2005) 15103-15110
113. McCloskey D.P., Hintz T.M., Pierce J.P., and Scharfman H.E. Stereological methods reveal the robust size and stability of ectopic hilar granule cells after pilocarpine-induced status epilepticus in the adult rat. European Journal of Neuroscience 24 (2006) 2203-2210
114. McIntyre D.C., and Kelly M.E. The parahippocampal cortices and kindling. Annals of the New York Academy of Sciences 911 (2000) 343-354
115. McKeown M.J., and McNamara J.O. When do epileptic seizures really begin?. Neuron 30 (2001) 1-3
116. McNair K., Broad J., Riedel G., Davies C.H., and Cobb S.R. Global changes in the hippocampal proteome following exposure to an enriched environment. Neuroscience 145 (2007) 413-422
117. Mlynarik M., Johansson B.B., and Jezova D. Enriched environment influences adrenocortical response to immune challenge and glutamate receptor gene expression in rat hippocampus. Annals of the New York Academy of Sciences 1018 (2004) 273-280
118. Mohammed A.K., Winblad B., Ebendal T., and Larkfors L. Environmental influence on behaviour and nerve growth factor in the brain. Brain Research 528 (1990) 62-72
119. Mohammed A.H., Henriksson B.G., Soderstrom S., Ebendal T., Olsson T., and Seckl J.R. Environmental influences on the central nervous system and their implications for the aging rat. Behavioural Brain Research 57 (1993) 183-191
120. Mohammed A.H., Zhu S.W., Darmopil S., Hjerling-Leffler J., Ernfors P., Winblad B., Diamond M.C., Eriksson P.S., and Bogdanovic N. Environmental enrichment and the brain. Progress in Brain Research 138 (2002) 109-133
121. Moncada D., and Viola H. Phosphorylation state of CREB in the rat hippocampus: a molecular switch between spatial novelty and spatial familiarity?. Neurobiology of Learning and Memory 86 (2006) 9-18
122. Mora F., Segovia G., and Del Arco A. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Research Review 55 (2007) 78-88
123. Moser M.B., Trommald M., Egeland T., and Andersen P. Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells. Journal of Comparative Neurology 380 (1997) 373-381
124. Murphy M., Greferath U., Nag N., Nithianantharajah J., and Wilson Y.M. Tracing functional circuits using c-Fos regulated expression of marker genes targeted to neuronal projections. Frontiers in Bioscience 9 (2004) 40-47
125. Nagerl U.V., Mody I., Jeub M., Lie A.A., Elger C.E., and 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. Journal of Neuroscience 20 (2000) 1831-1836
126. Naka F., Narita N., Okado N., and Narita M. Modification of AMPA receptor properties following environmental enrichment. Brain and Development 27 (2005) 275-278
127. Nichols J.A., Jakkamsetti V.P., Salgado H., Dinh L., Kilgard M.P., and Atzori M. Environmental enrichment selectively increases glutamatergic responses in layer II/III of the auditory cortex of the rat. Neuroscience 145 (2007) 832-840
128. Nilsson M., and Pekny M. Enriched environment and astrocytes in central nervous system regeneration. Journal of Rehabilitation Medicine 39 (2007) 345-352
129. Nilsson M., Perfilieva E., Johansson U., Orwar O., and Eriksson P.S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. Journal of Neurobiology 39 (1999) 569-578
130. Nishiyama A., Watanabe M., Yang Z., and Bu J. Identity, distribution, and development of polydendrocytes: NG2-expressing glial cells. Journal of Neurocytology 31 (2002) 437-455
131. Nithianantharajah J., and Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nature Review Neuroscience 7 (2006) 697-709
132. Nithianantharajah J., Levis H., and Murphy M. Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiology of Learning and Memory 81 (2004) 200-210
133. Nunn J.A., Graydon F.J., Polkey C.E., and Morris R.G. Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration. Brain 122 (1999) 47-59
134. Okazaki M.M., Evenson D.A., and Nadler J.V. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. Journal of Comparative Neurology 352 (1995) 515-534
135. Olson A.K., Eadie B.D., Ernst C., and Christie B.R. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16 (2006) 250-260
136. Pang T.Y., Stam N.C., Nithianantharajah J., Howard M.L., and Hannan A.J. Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience 141 (2006) 569-584
137. Parent J.M., and Lowenstein D.H. Mossy fiber reorganization in the epileptic hippocampus. Current Opinion in Neurology 10 (1997) 103-109
138. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. Journal of Neuroscience 17 (1997) 3727-3738
139. Parent J.M., Tada E., Fike J.R., and Lowenstein D.H. Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. Journal of Neuroscience 19 (1999) 4508-4519
140. Parent J.M., von dem Bussche N., and Lowenstein D.H. Prolonged seizures recruit caudal subventricular zone glial progenitors into the injured hippocampus. Hippocampus 16 (2006) 321-328
141. Passineau M.J., Green E.J., and Dietrich W.D. Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Experimental Neurology 168 (2001) 373-384
142. 2 and differential changes in somatostatin receptor messenger RNAs, binding sites and somatostatin release in kainic acid-treated rats. Neuroscience 65 (1995) 1087-1097
143. Pham T.M., Soderstrom S., Winblad B., and Mohammed A.H. Effects of environmental enrichment on cognitive function and hippocampal NGF in the non-handled rats. Behavioural Brain Research 103 (1999) 63-70
144. Pham T.M., Ickes B., Albeck D., Soderstrom S., Granholm A.C., and Mohammed A.H. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94 (1999) 279-286
145. Pham T.M., Winblad B., Granholm A.C., and Mohammed A.H. Environmental influences on brain neurotrophins in rats. Pharmacology, Biochemistry, and Behaviour 73 (2002) 167-175
146. Pierce J.P., Melton J., Punsoni M., McCloskey D.P., and Scharfman H.E. Mossy fibers are the primary source of afferent input to ectopic granule cells that are born after pilocarpine-induced seizures. Experimental Neurology 196 (2005) 316-331
147. Pinaud R., Penner M.R., Robertson H.A., and Currie R.W. Upregulation of the immediate early gene arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Brain Research Molecular Brain Research 91 (2001) 50-56
148. Poo M.M. Neurotrophins as synaptic modulators. Nature Review Neuroscience 2 (2001) 24-32
149. Raine A., Mellingen K., Liu J., Venables P., and Mednick S.A. Effects of environmental enrichment at ages 3-5 years on schizotypal personality and antisocial behavior at ages 17 and 23 years. American Journal of Psychiatry 160 (2003) 1627-1635
150. Rampon C., and Tsien J.Z. Genetic analysis of learning behavior-induced structural plasticity. Hippocampus 10 (2000) 605-609
151. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., Tsien J.Z., and Hu Y. Effects of environmental enrichment on gene expression in the brain. Proceedings of National Academy of Sciences USA 97 (2000) 12880-12884
152. Rampon C., Tang Y.P., Goodhouse J., Shimizu E., Kyin M., and Tsien J.Z. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nature Neuroscience 3 (2000) 238-244
153. Rao M.S., Hattiangady B., Abdel-Rahman A., Stanley D.P., and Shetty A.K. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. European Journal of Neuroscience 21 (2005) 464-476
154. Rao M.S., Hattiangady B., Reddy D.S., and Shetty A.K. Hippocampal neurodegeneration, spontaneous seizures, and mossy fiber sprouting in the F344 rat model of temporal lobe epilepsy. Journal of Neuroscience Research 83 (2006) 1088-1105
155. Rasmuson S., Olsson T., Henriksson B.G., Kelly P.A., Holmes M.C., Seckl J.R., and Mohammed A.H. Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Brain Research Molecular Brain Research 53 (1998) 285-290
156. Restivo L., Ferrari F., Passino E., Sgobio C., Bock J., Oostra B.A., Bagni C., and Ammassari-Teule M. Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proceedings of National Academy of Sciences USA 102 (2005) 11557-11562
157. Richardson M.P., Strange B.A., Thompson P.J., Baxendale S.A., Duncan J.S., and Dolan R.J. Pre-operative verbal memory fMRI predicts post-operative memory decline after left temporal lobe resection. Brain 127 (2004) 2419-2426
158. Rosenzweig E.S., and Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Progress in Neurobiology 69 (2003) 143-179
159. Rosenzweig M.R., and Bennett E.L. Cerebral changes in rats exposed individually to an enriched environment. Journal of Comparative Physiology and Psychology 80 (1972) 304-313
160. Rosenzweig M.R., and Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behavioural Brain Research 78 (1996) 57-65
161. Rosenzweig M.R., Krech D., Bennett E.L., and Diamond M.C. Effects of environmental complexity and training on brain chemistry and anatomy: a replication and extension. Journal of Comparative Physiology and Psychology 55 (1962) 429-437
162. Rosenzweig M.R., Krech D., Bennett E.L., and Zolman J.F. Variation in environmental complexity and brain measures. Journal of Comparative Physiology and Psychology 55 (1962) 1092-1095
163. Rosenzweig M.R., Bennett E.L., Diamond M.C., Wu S.Y., Slagle R.W., and Saffran E. Influences of environmental complexity and visual stimulation on development of occipital cortex in rat. Brain Research 14 (1969) 427-445
164. Rossi C., Angelucci A., Costantin L., Braschi C., Mazzantini M., Babbini F., Fabbri M.E., Tessarollo L., Maffei L., Berardi N., and Caleo M. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. European Journal of Neuroscience 24 (2006) 1850-1856
165. Rutten A., van Albada M., Silveira D.C., Cha B.H., Liu X., Hu Y.N., Cilio M.R., and Holmes G.L. Memory impairment following status epilepticus in immature rats: time-course and environmental effects. European Journal of Neuroscience 16 (2002) 501-513
166. Sahay A., and Hen R. Adult hippocampal neurogenesis in depression. Nature Neuroscience 10 (2007) 1110-1115
167. Saito S., Kobayashi S., Ohashi Y., Igarashi M., Komiya Y., and Ando S. Decreased synaptic density in aged brains and its prevention by rearing under enriched environment as revealed by synaptophysin contents. Journal of Neuroscience Research 39 (1994) 57-62
168. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., and Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
169. Scantlebury M.H., Heida J.G., Hasson H.J., Veliskova J., Velisek L., Galanopoulou A.S., and Moshe S.L. Age-dependent consequences of status epilepticus: animal models. Epilepsia 48 Suppl. 2 (2007) 75-82
170. Scharfman H.E. Brain-derived neurotrophic factor and epilepsy-a missing link?. Epilepsy Currents 5 (2005) 83-88
171. Scharfman H.E., Goodman J.H., and Sollas A.L. Actions of brain-derived neurotrophic factor in slices from rats with spontaneous seizures and mossy fiber sprouting in the dentate gyrus. Journal of Neuroscience 19 (1999) 5619-5631
172. Scharfman H.E., Goodman J.H., and Sollas A.L. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. Journal of Neuroscience 20 (2000) 6144-6158
173. Scharfman H.E., Goodman J.H., Sollas A.L., and Croll S.D. Spontaneous limbic seizures after intrahippocampal infusion of brain-derived neurotrophic factor. Experimental Neurology 174 2 (2002) 201-214
174. Scharfman H.E., Sollas A.L., and Goodman J.H. Spontaneous recurrent seizures after pilocarpine-induced status epilepticus activate calbindin-immunoreactive hilar cells of the rat dentate gyrus. Neuroscience 111 (2002) 71-81
175. Scharfman H.E., Sollas A.E., Berger R.E., Goodman J.H., and Pierce J.P. Perforant path activation of ectopic granule cells that are born after pilocarpine-induced seizures. Neuroscience 121 (2003) 1017-1029
176. Scharfman H., Goodman J., and McCloskey D. Ectopic granule cells of the rat dentate gyrus. Developmental Neuroscience 29 (2007) 14-27
177. Schneider T., Turczak J., and Przewlocki R. Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: issues for a therapeutic approach in autism. Neuropsychopharmacology 31 (2006) 36-46
178. Schridde U., and van Luijtelaar G. The influence of strain and housing on two types of spike-wave discharges in rats. Genes, Brain, and Behaviour 3 (2004) 1-7
179. Schwartz S. Effect of neonatal cortical lesions and early environmental factors on adult rat behavior. Journal of Comparative Physiology and Psychology 57 (1964) 72-77
180. Segal M. New building blocks for the dendritic spine. Neuron 31 (2001) 169-171
181. Shapiro L.A., and Ribak C.E. Integration of newly born dentate granule cells into adult brains: hypotheses based on normal and epileptic rodents. Brain Research Review 48 (2005) 43-56
182. Shapiro L.A., and Ribak C.E. Newly born dentate granule neurons after pilocarpine-induced epilepsy have hilar basal dendrites with immature synapses. Epilepsy Research 69 (2006) 53-66
183. Shapiro L.A., Korn M.J., and Ribak C.E. Newly generated dentate granule cells from epileptic rats exhibit elongated hilar basal dendrites that align along GFAP-immunolabeled processes. Neuroscience 136 (2005) 823-831
184. Shetty A.K. Entorhinal axons exhibit sprouting in CA1 subfield of the adult hippocampus in a rat model of temporal lobe epilepsy. Hippocampus 12 (2002) 534-542
185. Shetty A.K., and Hattiangady B. Restoration of calbindin after fetal hippocampal CA3 cell grafting into the injured hippocampus in a rat model of temporal lobe epilepsy. Hippocampus 17 (2007) 943-956
186. Shetty A.K., and Turner D.A. Development of fetal hippocampal grafts in intact and lesioned hippocampus. Progress in Neurobiology 50 (1996) 597-653
187. Shetty A.K., and Turner D.A. Fetal hippocampal cells grafted to kainate-lesioned CA3 region of adult hippocampus suppress aberrant supragranular sprouting of host mossy fibers. Experimental Neurology 143 (1997) 231-245
188. Shetty A.K., and Turner D.A. Aging impairs axonal sprouting response of dentate granule cells following target loss and partial deafferentation. Journal of Comparative Neurology 414 (1999) 238-254
189. Shetty A.K., and Turner D.A. Fetal hippocampal grafts containing CA3 cells restore host hippocampal glutamate decarboxylase-positive interneuron numbers in a rat model of temporal lobe epilepsy. Journal of Neuroscience 20 (2000) 8788-8801
190. Shetty A.K., and Turner D.A. Glutamic acid decarboxylase-67-positive hippocampal interneurons undergo a permanent reduction in number following kainic acid-induced degeneration of CA3 pyramidal neurons. Experimental Neurology 169 (2001) 276-297
191. Shetty A.K., Zaman V., and Turner D.A. Pattern of long-distance projections from fetal hippocampal field CA3 and CA1 cell grafts in lesioned CA3 of adult hippocampus follows intrinsic character of respective donor cells. Neuroscience 99 (2000) 243-255
192. Shetty A.K., Zaman V., and Shetty G.A. Hippocampal neurotrophin levels in a kainate model of temporal lobe epilepsy: a lack of correlation between brain-derived neurotrophic factor content and progression of aberrant dentate mossy fiber sprouting. Journal of Neurochemistry 87 (2003) 147-159
193. Shetty A.K., Zaman V., and Hattiangady B. Repair of the injured adult hippocampus through graft-mediated modulation of the plasticity of the dentate gyrus in a rat model of temporal lobe epilepsy. Journal of Neuroscience 25 (2005) 8391-8401
194. Siddiqui A.H., and Joseph S.A. CA3 axonal sprouting in kainate-induced chronic epilepsy. Brain Research 1066 (2005) 129-146
195. Sloviter R.S. The neurobiology of temporal lobe epilepsy: too much information, not enough knowledge. Comptes Rendus Biologies 328 (2005) 143-153
196. Spires T.L., Grote H.E., Varshney N.K., Cordery P.M., van Dellen A., Blakemore C., and Hannan A.J. Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. Journal of Neuroscience 24 (2004) 2270-2276
197. Sutula T., Cascino G., Cavazos J., Parada I., and Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Annals of Neurology 26 (1989) 321-330
198. Tang A.C., and Zou B. Neonatal exposure to novelty enhances long-term potentiation in CA1 of the rat hippocampus. Hippocampus 12 (2002) 398-404
199. Tang Y.P., Wang H., Feng R., Kyin M., and Tsien J.Z. Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology 41 (2001) 779-790
200. Tauck D.L., and Nadler J.V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. Journal of Neuroscience 5 (1985) 1016-1022
201. Terry R.D. Alzheimer's disease and the aging brain. Journal of Geriatric Psychiatry and Neurology 19 (2006) 125-128
202. Thoenen H. Neurotrophins and neuronal plasticity. Science 270 (1995) 593-598
203. Torasdotter M., Metsis M., Henriksson B.G., Winblad B., and Mohammed A.H. Expression of neurotrophin-3 mRNA in the rat visual cortex and hippocampus is influenced by environmental conditions. Neuroscience Letter 218 (1996) 107-110
204. Torasdotter M., Metsis M., Henriksson B.G., Winblad B., and Mohammed A.H. Environmental enrichment results in higher levels of nerve growth factor mRNA in the rat visual cortex and hippocampus. Behavioural Brain Research 93 (1998) 83-90
205. Turner D.A., and Shetty A.K. Clinical prospects for neural grafting therapy for hippocampal lesions and epilepsy. Neurosurgery 52 (2003) 632-644 (Discussion 634-641)
206. Turner C.A., Yang M.C., and Lewis M.H. Environmental enrichment: effects on stereotyped behavior and regional neuronal metabolic activity. Brain Research 938 (2002) 15-21
207. van Praag H., Kempermann G., and Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience 2 (1999) 266-270
208. van Praag H., Kempermann G., and Gage F.H. Neural consequences of environmental enrichment. Nature Review Neuroscience 1 (2000) 191-198
209. van Rijzingen I.M., Gispen W.H., and Spruijt B.M. Postoperative environmental enrichment attenuates fimbria-fornix lesion-induced impairments in Morris maze performance. Neurobiology of Learning and Memory 67 (1997) 21-28
210. Wallace C.S., Withers G.S., Weiler I.J., George J.M., Clayton D.F., and Greenough W.T. Correspondence between sites of NGFI-A induction and sites of morphological plasticity following exposure to environmental complexity. Brain Research Molecular Brain Research 32 (1995) 211-220
211. Wang, C.A., Lai, M.C., Lui, C.C., Yang, S.N., Tiao, M.M., Hsieh, C.S., Lin, H.H., Huang, L.T., 2007. An enriched environment improves cognitive performance after early-life status epilepticus accompanied by an increase in phosphorylation of extracellular signal-regulated kinase 2. Epilepsy Behaviour [Epub ahead of print] PMID: 17826356.
212. Wieser H.G. ILAE commission report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45 (2004) 695-714
213. Will B., Galani R., Kelche C., and Rosenzweig M.R. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Progress in Neurobiology 72 (2004) 167-182
214. Williams B.M., Luo Y., Ward C., Redd K., Gibson R., Kuczaj S.A., and McCoy J.G. Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiology and Behaviour 73 (2001) 649-658
215. Wozny C., Gabriel S., Jandova K., Schulze K., Heinemann U., and Behr J. Entorhinal cortex entrains epileptiform activity in CA1 in pilocarpine-treated rats. Neurobiology of Disease 19 (2005) 451-460
216. Wuarin J.P., and Dudek F.E. Excitatory synaptic input to granule cells increases with time after kainate treatment. Journal of Neurophysiology 85 (2001) 1067-1077
217. Young D., Lawlor P.A., Leone P., Dragunow M., and During M.J. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nature Medicine 5 (1999) 448-453
218. Zhu S.W., Yee B.K., Nyffeler M., Winblad B., Feldon J., and Mohammed A.H. Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behavioural Brain Research 169 (2006) 10-20