Opportunities for improving animal welfare in rodent models of epilepsy and seizures

Journal of Neuroscience Methods

Volumn 260, Issue , 2016, Pages 2-25

  Lidster, Katie ^a   Jefferys, John G ^b   Blümcke, Ingmar ^c   Crunelli, Vincenzo ^d   Flecknell, Paul ^e   Frenguelli, Bruno G ^f   Gray, William P ^g   Kaminski, Rafal ^h   Pitkänen, Asla ⁱ   Ragan, Ian ^a   Shah, Mala ^j   Simonato, Michele ^k   Trevelyan, Andrew ^e   Volk, Holger ^l   Walker, Matthew ^m   Yates, Neil ⁿ   Prescott, Mark J ^a  

^a National Centre for the Replacement   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f UNIVERSITY OF WARWICK   (United Kingdom)

^g CARDIFF UNIVERSITY   (United Kingdom)

^h UCB PHARMA   (Belgium)

ⁱ UNIVERSITY OF EASTERN FINLAND   (Finland)

^j UNIVERSITY OF LONDON   (United Kingdom)

^k UNIVERSITY OF FERRARA   (Italy)

^l ROYAL VETERINARY COLLEGE   (United Kingdom)

^m UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁿ UNIVERSITY OF NOTTINGHAM   (United Kingdom)

more..

Author keywords

3Rs; Animal model; Epilepsy; Mouse; Rat; Refinement; Seizure

Indexed keywords

ANTICONVULSIVE AGENT; BIOLOGICAL MARKER;

ANIMAL HOUSING; ANIMAL WELFARE; COMORBIDITY; DISTRESS SYNDROME; ENVIRONMENTAL ENRICHMENT; EPILEPSY; IN VIVO STUDY; METHODOLOGY; NONHUMAN; PAIN; PERIOPERATIVE PERIOD; PRIORITY JOURNAL; RECORDING; REVIEW; RODENT MODEL; SEIZURE; SYSTEMATIC REVIEW (TOPIC); ANIMAL; ANIMAL EXPERIMENT; DISEASE MODEL; ETHICS; MOUSE; PATHOPHYSIOLOGY; PRACTICE GUIDELINE; RAT; RODENT; STANDARDS; UNITED KINGDOM;

ANIMAL EXPERIMENTATION; ANIMAL WELFARE; ANIMALS; DISEASE MODELS, ANIMAL; EPILEPSY; GUIDELINES AS TOPIC; MICE; RATS; RODENTIA; UNITED KINGDOM;

EID: 84957433223     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2015.09.007     Document Type: Review

References (235)

1. Abraham J., Fox P.D., Condello C., Bartolini A., Koh S. Minocycline attenuates microglia activation and blocks the long-term epileptogenic effects of early-life seizures. Neurobiol Dis 2012, 46:425-430.
2. Akman O., Moshé S.L., Galanopoulou A.S. Early life status epilepticus and stress have distinct and sex-specific effects on learning, subsequent seizure outcomes, including anticonvulsant response to phenobarbital. CNS Neurosci Ther 2015, 21(2):181-192.
3. Ali A., Dua Y., Constance J.E., Franklin M.R., Dudek F.E. A once-per-day, drug-in-food protocol for prolonged administration of antiepileptic drugs in animal models. Epilepsia 2012, 53(1):199-206.
4. Annegers J.F., Hauser W.A., Coan S.P., Rocca W.A. A population-based study of seizures after traumatic brain injuries. N Engl J Med 1998, 338(1):20-24.
5. Arcieri S., Velotti R., Noe F., Carriero G., Cattalini A., Galbardi B., et al. Variable electrobehavioural patterns during focal nonconvulsive status epilepticus induced by unilateral intrahippocampal injection of kainic acid. Epilepsia 2014, 55(12):1978-1985.
6. Arndt S.S., Laarakker M.C., van Lith H.A., van der Staay F.J., Gieling E., Salomons A.R., et al. Individual housing of mice-impact on behaviour and stress responses. Physiol Behav 2009, 97:385-393.
7. Ashall V. Endpoint Matrix: a conceptual tool to promote consideration of the multiple dimensions of humane endpoints. ALTEX 2014, 31(2):209-213.
8. Auvergne R., Lere C., El Bahh B., Arthaud S., Lespinet V., Rougier A., et al. Delayed kindling epileptogenesis and increased neurogenesis in adult rats housed in an enriched environment. Brain Res 2002, 954(2):277-285.
9. Bagetta G., Corasaniti M., Nistico G., Bowery N. Behavioural and neuropathological effects produced by tetanus toxin injected into the hippocampus of rats. Neuropharmacology 1990, 29(8):765-770.
10. Bankstahl M., Muller C.J., Wilk E., Schughart K., Loscher W. Generation and characterization of pilocarpine-sensitive C57BL/6 mice as a model of temporal lobe epilepsy. Behav Brain Res 2012, 230(1):182-191.
11. Baran S., Froberg-Fejko K., Lecker J., Johnson E., Disselhorst D., Terreros D., et al. Post-surgical environmental enrichment in rodents. Enrich Rec 2010, 3:4-6.
12. Barkmeier D.T., Loeb J.A. An animal model to study the clinical significance of interictal spiking. Clin EEG Neurosci 2009, 40(4):234-238.
13. Bartolomucci A., Chirieleison A., Gioiosa L., Ceresini G., Parmigiani S., Palanza P. Age at group formation alters behavior and physiology in male but not female CD-1 mice. Physiol Behav 2004, 82:425-434.
14. Bartolomucci A., Palanza P., Gaspani L., Limiroli E., Panerai A.E., Ceresini G., et al. Social status in mice: behavioral, endocrine and immune changes are context dependent. Physiol Behav 2001, 73:401-410.
15. Bastlund J.F., Jennum P., Mohapel P., Vogel V., Watson W.P. Measurement of cortical and hippocampal epileptiform activity in freely moving rats by means of implantable radiotelemetry. J Neurosci Methods 2004, 138(1-2):65-72.
16. Bateson P., Johansen-Berg H., Jones D., Keverne E., Matthews P., Milner A., et al. Review of research using non-human primates: report of a panel chaired by Professor Sir Patrick Bateson FRS 2011, Wellcome Trust, London.
17. Baulac M., Pitkänen A. Research priorities in epilepsy for the next decade-a representative view of the European Scientific Community. Epilepsia 2008, 50:571-578.
18. Baumans V. Environmental enrichment for laboratory rodents and rabbits: requirements of rodents, rabbits, and research. ILAR J 2005, 46:162-170.
19. Baumans V. The laboratory mouse. The UFAW handbook on the care and management of laboratory and other research animals 2010, 276-310. Wiley-Blackwell, Oxford, UK. 8th ed. R. Hubrecht, J. Kirkwood (Eds.).
20. Baumans V., Brain P., Brugere H., Clausing T., Jeneskog T., Perretta G. Pain and distress in laboratory rodents and lagomorphs. Report of the Federation of European Laboratory Animal Science Associations (FELASA) Working Group on Pain and Distress accepted by the FELASA Board of Management November 1992. Lab Anim 1994, 28:97-112.
21. Belz E., Kennell J., Czambel R., Rubin R., Rhodes M. Environmental enrichment lowers stress-responsive hormones in single housed male and female rats. Pharmacol Biochem Behav 2003, 76:481-486.
22. Berdoy M. The laboratory rat: a natural history 2003, Available from: 〈http://www.ratlife.org/〉 [Internet].
23. Berg A.T., Berkovic S.F., Brodie M.J., Buchhalter J., Cross J.H., van Emde Boas W., et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia 2010, 51(4):676-685.
24. Berg A.T., Cross J.H. Towards a modern classification of the epilepsies?. Lancet Neurol 2010, 9(5):459-461.
25. Berg A.T., Scheffer I.E. New concepts in classification of the epilepsies: entering the 21st century. Epilepsia 2011, 52(6):1058-1062.
26. Bernard P.B., Castano A.M., O'Leary H., Simpson K., Browning M.D., Benke T.A. Phosphorylation of FMRP and alterations of FMRP complex underlie enhanced mLTD in adult rats triggered by early life seizures. Neurobiol Dis 2013, 59:1-17.
27. Blair R.E., Deshpande L.S., Holbert W.H., Churn S.B., DeLorenzo R.J. Age-dependent mortality in the pilocarpine model of status epilepticus. Neurosci Lett 2009, 453(3):233-237.
28. Boggiano M.M., Cavigelli S.A., Dorsey J.R., Kelley C.E.P., Ragan C.M., Chandler-Laney P.C. Effect of a cage divider permitting social stimuli on stress and food intake in rats. Physiol Behav 2008, 95:222-228.
29. Borges K., Gearing M., McDermott D.L., Smith A.B., Almonte A.G., Wainer B.H., et al. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp Neurol 2003, 182(1):21-34.
30. Bouilleret V., Ridoux V., Depaulis A., Marescaux C., Nehlig A., Le Gal La Salle G. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 1999, 89(3):717-729.
31. Bourdi M., Davies J.S., Pohl L.R. Mispairing C57BL/6 substrains of genetically engineered mice and wild-type controls can lead to confounding results as it did in studies of JNK2 in acetaminophen and concanavalin A liver injury. Chem Res Toxicol 2011, 24(6):794-796.
32. Brain P. What does individual housing mean to a mouse?. Life Sci 1975, 16:187-200.
33. Brooks-Kayal A.R., Bath K.G., Berg A.T., Galanopoulou A.S., Holmes G.L., Jensen F.E., et al. Issues related to symptomatic and disease-modifying treatments affecting cognitive and neuropsychiatric comorbidities of epilepsy. Epilepsia 2013, 4:44-60.
34. Caldecott-Hazard S., Liebeskind J.C. Test-specific analgesia elicited by kindled seizures in rats. Brain Res 1982, 251:196-199.
35. Caldecott-Hazard S., Shavit Y., Berman D.W., Liebeskind J.C. Seizure induced opioid and non-opioid analgesia in rats. Proc West Pharmacol Soc 1982, 25:107-111.
36. Camfield C., Camfield P. Juvenile myoclonic epilepsy 25 years after seizure onset: a population-based study. Neurology 2009, 73(13):1041-1045.
37. Castelhano A., Cassane G., Scorza F., Cysneiros R. Altered anxiety-related and abnormal social behaviors in rats exposed to early life seizures. Front Behav Neurosci 2013, 7:36.
38. Cavalheiro E.A., Leite J.P., Bortolotto Z.A., Turski W.A., Ikonomidou C., Turski L. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 1991, 32:778-782.
39. Chapman K., Sewell F., Allais L., Delongeas J.-L., Donald E., Festag M., et al. A global pharmaceutical company initiative: an evidence-based approach to define the upper limit of body weight loss in short term toxicity studies. Regul Toxicol Pharmacol 2013, 67:27-38.
40. Chen N., Liu C., Yan N., Hu W., Zhang J., Ge Y., et al. A macaque model of mesial temporal lobe epilepsy induced by unilateral intrahippocampal injection of kainic acid. PLoS ONE 2013, 8:e72336.
41. Chung J.-I., Kim A.Y., Lee S.H., Baik E.J. Seizure susceptibility in immature brain due to lack of COX-2-induced PGF2α. Exp Neurol 2013, 249:95-103.
42. Cilio M.R., Sogawa Y., Cha B.H., Liu X., Huang L.T., Holmes G.L. Long-term effects of status epilepticus in the immature brain are specific for age and model. Epilepsia 2003, 44(4):518-528.
43. Clayton J.A., Collins F.S. Policy: NIH to balance sex in cell and animal studies. Nature 2014, 509:282-283.
44. Coimbra N.C., Castro-Souza C., Segato E.N., Nora J.E., Herrero C.F., Tedeschi-Filho W., et al. Post-ictal analgesia: involvement of opioid, serotoninergic and cholinergic mechanisms. Brain Res 2001, 888(2):314-320.
45. Collier G.H., Johnson D.F., CyBulski K.A., McHale C.A. Activity patterns in rats (Rattus norvegicus) as a function of the cost of access to four resources. J Comp Psychol 1990, 104(Mar (1)):53-65.
46. Culley D.J., Baxter M.G., Crosby C.A., Yukhananov R., Crosby G. Impaired acquisition of spatial memory 2 weeks after isoflurane and isoflurane-nitrous oxide anesthesia in aged rats. Anesth Analg 2004, 99:1393-1397.
47. Cunliffe V.T., Baines R.A., Giachello C.N.G., Lin W.-H., Morgan A., Reuber M., et al. Epilepsy research methods update: understanding the causes of epileptic seizures and identifying new treatments using non-mammalian model organisms. Seizure 2014, 24:44-51.
48. Curia G., Longo D., Biagini G., Jones R.S., Avoli M. The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 2008, 172(2):143-157.
49. Czuczwar S.J., Frey H.-H. Effect of morphine and morphine-like analgesics on susceptibility to seizures in mice. Neuropharmacology 1986, 25(5):465-469.
50. D'Ambrosio R., Fairbanks J.P., Fender J.S., Born D.E., Doyle D.L., Miller J.W. Post-traumatic epilepsy following fluid percussion injury in the rat. Brain 2004, 127:304-314.
51. Danober L., Deransart C., Depaulis A., Vergnes M., Marescaux C. Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 1998, 55(1):27-57.
52. Desjardins D., Persinger M.A. Association between intermale social aggression and cellular density within the central amygdaloid nucleus in rats with lithium/pilocarpine-induced seizures. Percept Mot Ski 1995, 81(2):635-641.
53. Doheny H.C., Whittington M.A., Jefferys J.G.R., Patsalos P.N. A comparison of the efficacy of carbamazepine and the novel anti-epileptic drug levetiracetam in the tetanus toxin model of focal complex partial epilepsy. Br J Pharmacol 2002, 135:1425-1434.
54. Dugladze T., Maziashvili N., Borgers C., Gurgenidze S., Haussler U., Winkelmann A., et al. GABA(B) autoreceptor-mediated cell type-specific reduction of inhibition in epileptic mice. Proc Natl Acad Sci USA 2013, 110(37):15073-15078.
55. Eccles M., Mason J. How to develop cost-conscious guidelines. Health Technol Assess (Rockv) 2001, 5(16):1-69.
56. England M.J., Liverman C.T., Schultz A.M., Strawbridge L.M. Epilepsy across the spectrum 2012, National Academies Press (US), Washington, DC.
57. Englot D.J., Mishra A.M., Mansuripur P.K., Herman P., Hyder F., Blumenfeld H. Remote effects of focal hippocampal seizures on the rat neocortex. J Neurosci 2008, 28:9066-9081.
58. Englot D.J., Yang L., Hamid H., Danielson N., Bai X., Marfeo A., et al. Impaired consciousness in temporal lobe seizures: role of cortical slow activity. Brain 2010, 133:3764-3777.
59. Epps S.A., Weinshenker D. Rhythm and blues: animal models of epilepsy and depression comorbidity. Biochem Pharmacol 2013, 85:135-146.
60. Esclapez M., Hirsch J.C., Ben-Ari Y., Bernard C. Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 1999, 408:449-460.
61. European Union Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the Protection of Animals Used for Scientific Purposes OJ L276/33 2010, Official Journal of the European Union 276, Brussels.
62. Ewing S.G., Lipski W.J., Grace A.A., Winter C. An inexpensive, charge-balanced rodent deep brain stimulation device: a step-by-step guide to its procurement and construction. J Neurosci Methods 2013, 219:324-330.
63. Fares R.P., Belmeguenai A., Sanchez P.E., Kouchi H.Y., Bodennec J., Morales A., et al. Standardized environmental enrichment supports enhanced brain plasticity in healthy rats and prevents cognitive impairment in epileptic rats. PLoS ONE 2013, 8(1):e53888.
64. Faverjon S., Silveira D.C., Fu D.D., Cha B.H., Akman C., Hu Y., et al. Beneficial effects of enriched environment following status epilepticus in immature rats. Neurology 2002, 59(9):1356-1364.
65. Ferrari P.F., Palanza P., Parmigiani S., Rodgers R.J. Interindividual variability in Swiss male mice: relationship between social factors, aggression, and anxiety. Physiol Behav 1998, 63:821-827.
66. Fisher R.S., Acevedo C., Arzimanoglou A., Bogacz A., Cross J.H., Elger C.E., et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia 2014, 55(4):475-482.
67. Fisher R.S., van Emde Boas W., Blume W., Elger C., Genton P., Lee P., et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005, 46(4):470-472.
68. Flandera V., Nováková V., Rech F. Role of infection in development of experimental epileptic seizures in rats. Physiol Bohemoslov 1973, 22(2):209-212.
69. Fornari R.V., Wichmann R., Atsak P., Atucha E., Barsegyan A., Beldjoud H., et al. Rodent stereotaxic surgery and animal welfare outcome improvements for behavioral neuroscience. J Vis Exp 2012, 59:e3528.
70. Franke H., Kittner H. Morphological alterations of neurons and astrocytes and changes in emotional behavior in pentylenetetrazol-kindled rats. Pharmacol Biochem Behav 2001, 70(2-3):291-303.
71. Frankel W.N. Genetics of complex neurological disease: challenges and opportunities for modeling epilepsy in mice and rats. Trends Genet 2009, 25(8):361-367.
72. Freitas R.L., Ferreira C.M., Ribeiro S.J., Carvalho A.D., Elias-Filho D.H., Garcia-Cairasco N., et al. Intrinsic neural circuits between dorsal midbrain neurons that control fear-induced responses and seizure activity and nuclei of the pain inhibitory system elaborating postictal antinociceptive processes: a functional neuroanatomical and neuropharmacologi. Exp Neurol 2005, 191(2):225-242.
73. Galanopoulou A.S. Sex and epileptogenesis, introduction to the special issue. Neurobiol Dis 2014, 72 Pt B:123-124.
74. Galanopoulou A.S., Buckmaster P.S., Staley K.J., Moshe S.L., Perucca E., Engel J., et al. Identification of new epilepsy treatments: issues in preclinical methodology. Epilepsia 2012, 53(3):571-582.
75. Galanopoulou A.S., Moshe S.L. In search of epilepsy biomarkers in the immature brain: goals, challenges and strategies. Biomark Med 2011, 5(5):615-628.
76. Galanopoulou A.S., Simonato M., French J.A., O'Brien T.J. Joint AES/ILAE translational workshop to optimize preclinical epilepsy research. Epilepsia 2013, 54:1-2.
77. Giorgi F.S., Galanopoulou A.S., Moshé S.L. Sex dimorphism in seizure-controlling networks. Neurobiol Dis 2014, 72:144-152.
78. Glien M., Brandt C., Potschka H., Voigt H., Ebert U., Loscher W. Repeated low-dose treatment of rats with pilocarpine: low mortality but high proportion of rats developing epilepsy. Epilepsy Res 2001, 46(2):111-119.
79. Gouveia K., Hurst J.L. Reducing mouse anxiety during handling: effect of experience with handling tunnels. PLoS ONE 2013, 8:e66401.
80. Grabenstatter H.L., Clark S., Dudek F.E. Anticonvulsant effects of carbamazepine on spontaneous seizures in rats with kainate-induced epilepsy: comparison of intraperitoneal injections with drug-in-food protocols. Epilepsia 2007, 48(12):2287-2295.
81. Graber K.D., Prince D.A. Chronic partial cortical isolation. Model seziures epilepsy 2005, 477-493. Academic Press, Waltham. A. Pitkänen, P.A. Schwartzkroin, S.L. Moshé (Eds.).
82. Grone B.P., Baraban S.C. Animal models in epilepsy research: legacies and new directions. Nat Neurosci 2015, 18(Feb (3)):339-343.
83. Guerrini R., Marini C., Mantegazza M. Genetic epilepsy syndromes without structural brain abnormalities: clinical features and experimental models. Neurotherapeutics 2014, 11:269-285.
84. Guo Q., Kuang P. Effect of qingyangshen on hippocampal alpha- and beta-tubulin gene expression during kainic acid induced epileptogenesis. J Tradit Chin Med 1993, 13(4):281-286.
85. Hannan A.J. Environmental enrichment and brain repair: harnessing the therapeutic effects of cognitive stimulation and physical activity to enhance experience-dependent plasticity. Neuropathol Appl Neurobiol 2013, 40:13-25.
86. Harhausen D., Sudmann V., Khojasteh U., Muller J., Zille M., Graham K., et al. Specific imaging of inflammation with the 18 kDa translocator protein ligand DPA-714 in animal models of epilepsy and stroke. PLoS ONE 2013, 8(8):e69529.
87. Haseman J.K., Bourbina J., Eustis S.L. Effect of individual housing and other experimental design factors on tumor incidence in B6C3F1 mice. Fundam Appl Toxicol 1994, 23:44-52.
88. Hashem A., Frey H.H. The effect of neuroleptics and neuroleptic/analgesic combinations on the sensitivity to seizures in mice. Anaesthesist 1988, 37(10):631-635.
89. Hatch A., G.W., Balazs T. Long-term isolation stress in rats. Science 1963, 142:507.
90. Hau J. Humane endpoints and the importance of training. Humane endpoints in animal experiments for biomedical research 1999, 71-74. Royal Society of Medicine Press, London.
91. Hawkins P. Progress in assessing animal welfare in relation to new legislation: opportunities for behavioural researchers. J Neurosci Methods 2014, 234:135-138.
92. Hawkins P., Morton D.B., Bevan R., Heath K., Kirkwood J., Pearce P., et al. Husbandry refinements for rats, mice, dogs and non-human primates used in telemetry procedures. Seventh report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement, Part B. Lab Anim 2004, 38(1):1-10.
93. Hawkins P., Morton D.B., Burman O., Dennison N., Honess P., Jennings M., et al. A guide to defining and implementing protocols for the welfare assessment of laboratory animals: eleventh report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Lab Anim 2011, 45(1):1-13.
94. Hayes K.E., Raucci J.A., Gades N.M., Toth L.A. An evaluation of analgesic regimens for abdominal surgery in mice. Contemp Top Lab Anim Sci 2000, 39:18-23.
95. Heinrichs S.C., Seyfried T.N. Behavioral seizure correlates in animal models of epilepsy: a road map for assay selection, data interpretation, and the search for causal mechanisms. Epilepsy Behav 2006, 8:5-38.
96. Hellier J.L., Dudek F.E. Chemoconvulsant model of chronic spontaneous seizures. Curr Protoc Neurosci 2005, 9(9):1-9.
97. Hellier J.L., Patrylo P.R., Buckmaster P.S., Dudek F.E. Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res 1998, 31(1):73-84.
98. Hendriksen C., Morton D., Cussler K. Use of humane end points to minimise suffering. The cost manual of laboratory animal care and use 2011, 333-353. CRC Press, Florida, USA. B. Howard, T. Nevalainen, G. Perretta (Eds.).
99. Hickman D.L., Swan M. Use of a body condition score technique to assess health status in a rat model of polycystic kidney disease. J Am Assoc Lab Anim Sci 2010, 49:155-159.
100. Home Office Guidance on the Operation of the Animals (Scientific Procedures) Act 1986 2014.
101. Honndorf S., Lindemann C., Tollner K., Gernert M. Female Wistar rats obtained from different breeders vary in anxiety-like behavior and epileptogenesis. Epilepsy Res 2011, 94(1-2):26-38.
102. Huang L., van Luijtelaar G. The effects of responsive and scheduled subicular high frequency stimulation in the intra-hippocampal kainic acid seizure model. Epilepsy Res 2013, 106(3):326-337.
103. Huang X., McMahon J., Huang Y. Rapamycin attenuates aggressive behavior in a rat model of pilocarpine-induced epilepsy. Neuroscience 2012, 215:90-97.
104. Hubrecht R., Kirkwood J. The UFAW handbook on the care and management of laboratory and other research animals 2010, Wiley-Blackwell, London. 8th ed.
105. Hurst J.L., Barnard C.J., Nevison C.M., West C.D. Housing and welfare in laboratory rats: welfare implications of isolation and social contact among caged males. Anim Welf 1997, 6:329-347.
106. Hurst J.L., West R.S. Taming anxiety in laboratory mice. Nat Methods 2010, 7(10):825-826.
107. Inostroza M., Cid E., Brotons-Mas J., Gal B., Aivar P., Uzcategui Y.G., et al. Hippocampal-dependent spatial memory in the water maze is preserved in an experimental model of temporal lobe epilepsy in rats. PLoS ONE 2011, 6(7):26.
108. Inostroza M., Cid E., Menendez de la Prida L., Sandi C. Different emotional disturbances in two experimental models of temporal lobe epilepsy in rats. PLoS ONE 2012, 7(6):e38959.
109. Jedrzejko C., Persinger M.A. Weight gain in post-seized rats is facilitated by adding aspirin, glucose, or glucose-taurine-acetaminophen to food mush. Psychol Rep 2001, 89(1):188-190.
110. Jimenez-Pacheco A., Mesuret G., Sanz-Rodriguez A., Tanaka K., Mooney C., Conroy R., et al. Increased neocortical expression of the P2X7 receptor after status epilepticus and anticonvulsant effect of P2X7 receptor antagonist A-438079. Epilepsia 2013, 54(9):1551-1561.
111. Jirkof P. Effects of experimental housing conditions on recovery of laboratory mice. Lab Anim 2015, 44(2):65-70.
112. Jones H., Oates J., Trussell B. An applied approach to the assessment of severity. Humane endpoints in animal experiments for biomedical research 1999, 40-47. Royal Society of Medicine Press, Royal Society for Medicine Press Ltd, London. C. Hendriksen, D. Morton (Eds.).
113. Jones N.C., Salzberg M.R., Kumar G., Couper A., Morris M.J., O'Brien T.J. Elevated anxiety and depressive-like behavior in a rat model of genetic generalized epilepsy suggesting common causation. Exp Neurol 2008, 209(1):254-260.
114. Kalliokoski O., Teilmann A.C., Jacobsen K.R., Abelson K.S.P., Hau J. The lonely mouse-single housing affects serotonergic signaling integrity measured by 8-OH-DPAT-induced hypothermia in male mice. PLoS ONE 2014, 9:e111065.
115. Kalynchuk L.E., Pinel J.P., Treit D. Characterization of the defensive nature of kindling-induced emotionality. Behav Neurosci 1999, 113(4):766-775.
116. Kilkenny C., Browne W.J., Cuthill I.C., Emerson M., Altman D.G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010, 8(6):e1000412.
117. Kilkenny C., Parsons N., Kadyszewski E., Festing M.F., Cuthill I.C., Fry D., et al. Survey of the quality of experimental design, statistical analysis and reporting of research using animals. PLoS ONE 2009, 4(11):e7824.
118. Koh S., Magid R., Chung H., Stine C.D., Wilson D.N. Depressive behavior and selective down-regulation of serotonin receptor expression after early-life seizures: reversal by environmental enrichment. Epilepsy Behav 2007, 10(1):26-31.
119. Koppel B.S., Harden C.L. Gender issues in the neurobiology of epilepsy: A clinical perspective. Neurobiol Dis 2014, 72 Part B:193-197.
120. Kotloski R.J., Sutula T.P. Environmental enrichment: Evidence for an unexpected therapeutic influence. Exp Neurol 2014, 264C:121-126.
121. Kulesskaya N., Rauvala H., Voikar V. Evaluation of social and physical enrichment in modulation of behavioural phenotype in C57BL/6J female mice. PLoS ONE 2011, 6:e24755.
122. Langford D.J., Bailey A.L., Chanda M.L., Clarke S.E., Drummond T.E., Echols S., et al. Coding of facial expressions of pain in the laboratory mouse. Nat Methods 2010, 7(6):447-449.
123. Latham N., Mason G. From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl Anim Behav Sci 2004, 86:261-289.
124. Leach M.C., Klaus K., Miller A.L., Scotto di Perrotolo M., Sotocinal S.G., Flecknell P.A. The assessment of post-vasectomy pain in mice using behaviour and the Mouse Grimace Scale. PLoS ONE 2012, 7:e35656.
125. Leclercq K., Kaminski R.M. Genetic background of mice strongly influences treatment resistance in the 6 Hz seizure model. Epilepsia 2014, 56:310-318.
126. Lévesque M., Avoli M. The kainic acid model of temporal lobe epilepsy. Neurosci Biobehav Rev 2013, 37:2887-2899.
127. Lewis M.H. Environmental complexity and central nervous system development and function. Ment Retard Dev Disabil Res Rev 2004, 10(2):91-95.
128. Li Z., Li B., Zhu X., Yin P., Liu J., Huang S., et al. Neuroprotective effects of anti-high-mobility group box 1 antibody in juvenile rat hippocampus after kainic acid-induced status epilepticus. Neuroreport 2013, 24(14):785-790.
129. Liu Z., Gatt A., Werner S.J., Mikati M.A., Holmes G.L. Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res 1994, 19:191-204.
130. Long J.J., Shen B., Luo T., Stewart L., McMurran T.J., Leung L.S. Pilocarpine model of temporal lobe epilepsy shows enhanced response to general anesthetics. Exp Neurol 2009, 219(1):308-318.
131. Longo B., Covolan L., Chadi G., Mello L.E.A.M. Sprouting of mossy fibers and the vacating of postsynaptic targets in the inner molecular layer of the dentate gyrus. Exp Neurol 2003, 181:57-67.
132. Van Loo P., De Groot A., Van Zutphen L., Baumans V. Do male mice prefer or avoid each other's company? Influence of hierarchy, kinship and familiarity. J Appl Anim Welf Sci 2001, 4:91-103.
133. Van Loo P., Van de Weerd H., Van Zutphen L., Baumans V. Preference for social contact versus environmental enrichment in male laboratory mice. Lab Anim 2004, 38(2):178-188.
134. Van Loo P.L.P., Kuin N., Sommer R., Avsaroglu H., Pham T., Baumans V. Impact of "living apart together" on postoperative recovery of mice compared with social and individual housing. Lab Anim 2007, 41:441-455.
135. Löscher W. The pharmacokinetics of antiepileptic drugs in rats: consequences for maintaining effective drug levels during prolonged drug administration in rat models of epilepsy. Epilepsia 2007, 48(7):1245-1258.
136. Löscher W., Brandt C. Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev 2010, 62(4):668-700.
137. Löscher W., Klitgaard H., Twyman R.E., Schmidt D. New avenues for anti-epileptic drug discovery and development. Nat Rev Drug Discov 2013, 12(10):757-776.
138. Van Luijtelaar G. The prevention of behavioral consequences of idiopathic generalized epilepsy: evidence from rodent models. Neurosci Lett 2011, 497:177-184.
139. Van Luijtelaar G., Zobeiri M. Progress and outlooks in a genetic absence epilepsy model (WAG/Rij). Curr Med Chem 2014, 21:704-721.
140. Lüttjohann A., Fabene P.F., van Luijtelaar G. A revised Racine's scale for PTZ-induced seizures in rats. Physiol Behav 2009, 98:579-586.
141. Maheshwari A., Noebels J.L. Monogenic models of absence epilepsy: windows into the complex balance between inhibition and excitation in thalamocortical microcircuits. Prog Brain Res 2014, 213:223-252.
142. Manno I., Macchi F., Caleo M., Bozzi Y. Environmental enrichment reduces spontaneous seizures in the Q54 transgenic mouse model of temporal lobe epilepsy. Epilepsia 2011, 52(9):e113-e117.
143. Manser C., Broom D., Overend P., Morris T. Investigation into the preference of laboratory rats for nest-boxes and nesting materials. Lab Anim 1998, 32:23-35.
144. Manser C., Broom D., Overend P., Morris T. Operant studies to determine the strength of preference in laboratory rats for nest-boxes and nesting materials. Lab Anim 1998, 32(1):36-41.
145. Manser C.E., Elliot H., Morris T.H., Broom D.M. The use of a novel operant test to determine the strength of preference for flooring in laboratory rats. Lab Anim 1996, 30(1):1-6.
146. Mantegazza M., Rusconi R., Scalmani P., Avanzini G., Franceschetti S. Epileptogenic ion channel mutations: from bedside to bench and, hopefully, back again. Epilepsy Res 2010, 92:1-29.
147. Mareš J., Rokyta R. Algesthesia after epileptic seizure. Physiol Res 2009, 58(2):279-285.
148. Mareš P. Models of epileptic seizures in immature rats. Physiol Res 2012, 61:S103-S108.
149. Mareš P. Age and activation determines the anticonvulsant effect of ifenprodil in rats. Naunyn Schmiedebergs Arch Pharmacol 2014, 387(8):753-761.
150. Martin B.S., Kapur J. A combination of ketamine and diazepam synergistically controls refractory status epilepticus induced by cholinergin stimulation. Epilepsia 2008, 49(2):248-255.
151. Martin B., Ji S., Maudsley S., Mattson M.P. "Control" laboratory rodents are metabolically morbid: why it matters. Proc Natl Acad Sci USA 2010, 107(14):6127-6133.
152. Mazarati A.M., Shin D., Kwon Y.S., Bragin A., Pineda E., Tio D., et al. Elevated plasma corticosterone level and depressive behavior in experimental temporal lobe epilepsy. Neurobiol Dis 2009, 34:457-461.
153. McIntyre D.C. The kindling phenomenon. Models of seizures and epilepsy 2005, 351-363. Academic Press, Waltham. A. Pitkänen, P.A. Schwartzkroin, S.L. Moshé (Eds.).
154. McKhann G.M., Wenzel H.J., Robbins C.A., Sosunov A.A., Schwartzkroin P.A. Mouse strain differences in kainic acid sensitivity, seizure behavior, mortality, and hippocampal pathology. Neuroscience 2003, 122(2):551-561.
155. McLin J.P., Steward O. Comparison of seizure phenotype and neurodegeneration induced by systemic kainic acid in inbred, outbred, and hybrid mouse strains. Eur J Neurosci 2006, 24:2191-2202.
156. Meijer M., Kramer K., Remie R., Spruijt B., van Zutphen L., Baumans V. The effect of routine experimental procedures on physiological parameters in mice kept under different husbandry conditions. Anim Welf 2006, 15:31-38.
157. Mellanby J., George G., Robinson A., Thompson P. Epileptiform syndrome in rats produced by injecting tetanus toxin into the hippocampus. J Neurol Neurosurg Psychiatry 1977, 40(4):404-414.
158. Mellanby J., Oliva M., Peniket A., Nicholls B. The effect of experimental epilepsy induced by injection of tetanus toxin into the amygdala of the rat on eating behaviour and response to novelty. Behav Brain Res 1999, 100(1-2):113-122.
159. Mellanby J., Strawbridge P., Collingridge G.I., George G., Rands G., Stroud C., et al. Behavioural correlates of an experimental hippocampal epileptiform syndrome in rats. J Neurol Neurosurg Psychiatry 1981, 44(12):1084-1093.
160. Morelli E., Ghiglieri V., Pendolino V., Bagetta V., Pignataro A., Fejtova A., et al. Environmental enrichment restores CA1 hippocampal LTP and reduces severity of seizures in epileptic mice. Exp Neurol 2014, 261:320-327.
161. Morton D.B. Humane endpoints in animal experimentation for biomedical research: ethical, legal and practical aspects. Humane endpoints in animal experiments for biomedical research 1999, 5-12. Royal Society of Medicine Press, London, London; 1999.
162. Morton D.B. A systematic approach for establishing humane endpoints. ILAR J 2000, 41(2):80-86.
163. Morton D.B., Hawkins P., Bevan R., Heath K., Kirkwood J., Pearce P., et al. Refinements in telemetry procedures. Seventh report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement, Part A. Lab Anim 2003, 37:261-299.
164. Morton D.B., Jennings M., Buckwell A., Ewbank R., Godfrey C., Holgate B., et al. Refining procedures for the administration of substances. Report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Lab Anim 2001, 35(1):1-41.
165. Müller C.J., Gröticke I., Hoffmann K., Schughart K., Löscher W. Differences in sensitivity to the convulsant pilocarpine in substrains and sublines of C57BL/6 mice. Genes Brain Behav 2009, 8:481-492.
166. National Research Council Guide for the care and use of laboratory animals 2011, The National Academies Press, Washington. 8th ed.
167. Oliver V., De Rantere D., Ritchie R., Chisholm J., Hecker K.G., Pang D.S.J. Psychometric assessment of the Rat Grimace Scale and development of an analgesic intervention score. PLoS ONE 2014, 9:e97882.
168. Olsson I.A.S., Dahlborn K. Improving housing conditions for laboratory mice: a review of "environmental enrichment". Lab Anim 2002, 36:243-270.
169. Panayiotopoulos C.P. A clinical guide to epileptic syndromes and their treatment 2007, Springer, London. 2nd ed.
170. Park D.-W., Schendel A.A., Mikael S., Brodnick S.K., Richner T.J., Ness J.P., et al. Graphene-based carbon-layered electrode array technology for neural imaging and optogenetic applications. Nat Commun 2014, 5:5258.
171. Perez-Mendes P., Blanco M.M., Calcagnotto M.E., Cinini S.M., Bachiega J., Papoti D., et al. Modeling epileptogenesis and temporal lobe epilepsy in a non-human primate. Epilepsy Res 2011, 96:45-57.
172. Persinger M.A. Enhancement of limbic seizures by nocturnal application of experimental magnetic fields that simulate the magnitude and morphology of increases in geomagnetic activity. Int J Neurosci 1996, 86:271-280.
173. Persinger M.A., Makarec K., Bradley J.C. Characteristics of limbic seizures evoked by peripheral injections of lithium and pilocarpine. Physiol Behav 1988, 44(1):27-37.
174. Perucca E., Battino D., Tomson T. Gender issues in antiepileptic drug treatment. Neurobiol Dis 2014, 72 Part B:217-223.
175. Peters H.C., Hu H., Pongs O., Storm J.F., Isbrandt D. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat Neurosci 2005, 8(1):51-60.
176. Pierson M.G., Swann J.W. The sensitive period and optimum dosage for induction of audiogenic seizure susceptibility by kanamycin in the Wistar rat. Hear Res 1988, 32(1):1-10.
177. Pitkänen A., Huusko N., Ndode-Ekane X.E., Kyyriäinen J., Lipponen A., Lipsanen A., et al. Gender issues in antiepileptogenic treatments. Neurobiol Dis 2014, 72:224-232.
178. Pitkänen A., Immonen R. Epilepsy related to traumatic brain injury. Neurotherapeutics 2014, 11:286-296.
179. Pitkänen A., Nehlig A., Brooks-Kayal A.R., Dudek F.E., Friedman D., Galanopoulou A.S., et al. Issues related to development of antiepileptogenic therapies. Epilepsia 2013, 54:35-43.
180. Pitkänen A., Schwartzkroin P.A., Moshe S.L. Models of seizures and epilepsy 2006, Academic Press, Waltham.
181. Poole T. Happy animals make good science. Lab Anim 1997, 31:116-124.
182. Prescott M.J. Ethics of primate use. Adv Sci Res 2010, 5(Nov (1)):11-22. (Copernicus GmbH).
183. Prescott M.J., Brown V.J., Flecknell P.A., Gaffan D., Garrod K., Lemon R.N., et al. Refinement of the use of food and fluid control as motivational tools for macaques used in behavioural neuroscience research: report of a Working Group of the NC3Rs. J Neurosci Methods 2010, 193(Nov (2)):167-188.
184. Qiao X., Werkman T.R., Gorter J.A., Wadman W.J., van Vliet E.A. Expression of sodium channel alpha subunits 1.1, 1.2 and 1.6 in rat hippocampus after kainic acid-induced epilepsy. Epilepsy Res 2013, 106(1-2):17-28.
185. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephal Clin Neurophysiol 1972, 32:281-294.
186. Richardson C.A., Flecknell P. Anaesthesia and post-operative analgesia following experimental surgery in laboratory rodents: are we making progress?. Altern Lab Anim: ATLA 2005, 33(3):119-127.
187. Rice A.S.C., Cimino-Brown D., Eisenach J.C., Kontinen V.K., Lacroix-Fralish M.L., Machin I., et al. Animal models and the prediction of efficacy in clinical trials of analgesic drugs: a critical appraisal and call for uniform reporting standards. Pain 2008, 139(Oct (2)):243-247.
188. Riljak V., Marešová D., Pokorný J., Jandová K. Subconvulsive dose of kainic acid transiently increases the locomotor activity of adult Wistar rats. Physiol Res 2014, 64(2):263-267.
189. Robinson V., Morton D., Anderson D., Carver J., Francis R., Hubercht R., et al. Refinement and reduction in the production of genetically modified mice: sixth report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Altern Lab Anim 2004, 32(Jun (Suppl 1)):373-375.
190. Rutten A., van Albada M., Silveira D.C., Cha B.H., Liu X., Hu Y.N., et al. Memory impairment following status epilepticus in immature rats: time-course and environmental effects. Eur J Neurosci 2002, 16(3):501-513.
191. Scharfman H.E., Goodman J.H., Rigoulot M.-A., Berger R.E., Walling S.G., Mercurio T.C., et al. Seizure susceptibility in intact and ovariectomized female rats treated with the convulsant pilocarpine. Exp Neurol 2005, 196(Nov (1)):73-86.
192. Scharfman H.E., MacLusky N.J. Sex differences in the neurobiology of epilepsy: a preclinical perspective. Neurobiol Dis 2014, 72:180-192.
193. Schauwecker P.E. The relevance of individual genetic background and its role in animal models of epilepsy. Epilepsy Res 2011, 97(Nov (1-2)):1-11.
194. Schridde U., van Luijtelaar G. The influence of strain and housing on two types of spike-wave discharges in rats. Genes Brain Behav 2004, 3(1):1-7.
195. Sena E.S., van der Worp H.B., Bath P.M., Howells D.W., Macleod M.R. Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol 2010, 8(3):e1000344.
196. Shavit Y., Fish G., Wolf G., Mayburd E., Meerson Y., Yirmiya R., et al. The effects of perioperative pain management techniques on food consumption and body weight after laparotomy in rats. Anesth Analg 2005, 101(Oct (4)):1112-1116.
197. Sherwin C., Nicol C. Behavioural demand functions of caged laboratory mice for additional space. Anim Behav 1997, 53(1):67-74.
198. Shetty A.K., Hattiangady B., Rao M.S., Shuai B. Neurogenesis response of middle-aged hippocampus to acute seizure activity. PLoS ONE 2012, 7(8):e43286.
199. Sillanpää M., Shinnar S. Long-term mortality in childhood-onset epilepsy. N Engl J Med 2010, 363(Dec (26)):2522-2529.
200. Simeone K.A., Matthews S.A., Samson K.K., Simeone T.A. Targeting deficiencies in mitochondrial respiratory complex I and functional uncoupling exerts anti-seizure effects in a genetic model of temporal lobe epilepsy and in a model of acute temporal lobe seizures. Exp Neurol 2014, 251:84-90.
201. Simonato M., Brooks-Kayal A.R., Engel J., Galanopoulou A.S., Jensen F.E., Moshé S.L., et al. The challenge and promise of anti-epileptic therapy development in animal models. Lancet Neurol 2014, 13(9):949-960.
202. Sotocinal S.G., Sorge R.E., Zaloum A., Tuttle A.H., Martin L.J., Wieskopf J.S., et al. The Rat Grimace Scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions. Mol Pain 2011, Jan (7):55.
203. Sperber E.F., Haas K.Z., Romero M.T., Stanton P.K. Flurothyl status epilepticus in developing rats: behavioral, electrographic histological and electrophysiological studies. Brain Res Dev Brain Res 1999, 116(1):59-68.
204. Stables J.P., Bertram E., Dudek F.E., Holmes G., Mathern G., Pitkanen A., et al. Therapy discovery for pharmacoresistant epilepsy and for disease-modifying therapeutics: summary of the NIH/NINDS/AES models II workshop. Epilepsia 2003, 44(12):1472-1478.
205. Stafstrom C.E., Chronopoulos A., Thurber S., Thompson J.L., Holmes G.L. Age-dependent cognitive and behavioral deficits after kainic acid seizures. Epilepsia 1993, 34(3):420-432.
206. Stewart L.S., Cortez M.A., Snead O.C. Environmental enrichment improves behavioral outcome in the AY-9944 model of childhood atypical absence epilepsy. Int J Neurosci 2012, 122(8):449-457.
207. Stokes E.L., Flecknell P.A., Richardson C.A. Reported analgesic and anaesthetic administration to rodents undergoing experimental surgical procedures. Lab Anim 2009, 43(Apr (2)):149-154.
208. Sunderam S., Chernyy N., Peixoto N., Mason J.P., Weinstein S.L., Schiff S.J., et al. Improved sleep-wake and behavior discrimination using MEMS accelerometers. J Neurosci Methods 2007, 163(Jul (2)):373-383.
209. Szabó C.Á., Knape K.D., Leland M.M., Cwikla D.J., Williams-Blangero S., Williams J.T. Epidemiology and characterization of seizures in a pedigreed baboon colony. Comp Med 2012, 62(Dec (6)):535-538.
210. Tabb K., Boss-Williams K.A., Weiss J.M., Weinshenker D. Rats bred for susceptibility to depression-like phenotypes have higher kainic acid-induced seizure mortality than their depression-resistant counterparts. Epilepsy Res 2007, 74(2-3):140-146.
211. Thompson J.L., Carl F.G., Holmes G.L. Effects of age on seizure susceptibility in genetically epilepsy-prone rats (GEPR-9s). Epilepsia 1991, 32(2):161-167.
212. Tremoleda J.L., Kerton A., Gsell W. Anaesthesia and physiological monitoring during in vivo imaging of laboratory rodents: considerations on experimental outcomes and animal welfare. EJNMMI Res 2012, 2(1):44.
213. Turski L., Ikonomidou C., Turski W.A., Bortolotto Z.A., Cavalheiro E.A. Review: cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy. Synapse 1989, 3:154-171.
214. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav Brain Res 1983, 9(3):315-335.
215. Ullman-Culleré M.H., Foltz C.J. Body condition scoring: a rapid and accurate method for assessing health status in mice. Lab Anim Sci 1999, 49:319-323.
216. Vesterinen H.M., Sena E.S., Ffrench-Constant C., Williams A., Chandran S., Macleod M.R. Improving the translational hit of experimental treatments in multiple sclerosis. Mult Scler 2010, 16(9):1044-1055.
217. Viventi J., Kim D.H., Moss J.D., Kim Y.S., Blanco J.A., Annetta N., et al. A conformal, bio-interfaced class of silicon electronics for mapping cardiac electrophysiology. Sci Transl Med 2010, 2(24):24ra22.
218. Van Vlissingen J.M.F., Kuijpers M.H.M., van Oostrum E.C.M., Beems R.B., van Dijk J.E. Retrospective evaluation of clinical signs, pathology and related discomfort in chronic studies. Humane endpoints in animal experiments for biomedical research 1999, 89-94. Royal Society of Medicine Press, London.
219. Võikar V., Polus A., Vasar E., Rauvala H. Long-term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences. Genes Brain Behav 2005, 4:240-252.
220. Wang D.D., Englot D.J., Garcia P.A., Lawton M.T., Young W.L. Minocycline- and tetracycline-class antibiotics are protective against partial seizures in vivo. Epilepsy Behav 2012, 24(3):314-318.
221. Wasterlain C.G., Gloss D.S., Niquet J., Wasterlain A.S. Epileptogenesis in the developing brain. Handb Clin Neurol 2013, 111:427-439.
222. Van de Weerd H.A., Bulthuis R.J.A., Bergman A.F., Schlingmann F., Tolboom J., Van Loo P.L.P., et al. Validation of a new system for the automatic registration of behaviour in mice and rats. Behav Processes 2001, 53:11-20.
223. Weiergraber M., Henry M., Hescheler J., Smyth N., Schneider T. Electrocorticographic and deep intracerebral EEG recording in mice using a telemetry system. Brain Res Protoc 2005, 14(3):154-164.
224. Williams P., White A., Ferraro D., Clark S., Staley K., Dudek F.E. The use of radiotelemetry to evaluate electrographic seizures in rats with kainate-induced epilepsy. J Neurosci Methods 2006, 155:39-48.
225. Wolfensohn S., Hawkins P., Lilley E., Anthony D., Chambers C., Lane S., et al. Reducing suffering in animal models and procedures involving seizures, convulsions and epilepsy. J Pharmacol Toxicol Methods 2013, 67(1):9-15.
226. Wozniak D.F., Stewart G.R., Miller J.P., Olney J.W. Age-related sensitivity to kainate neurotoxicity. Exp Neurol 1991, 114(2):250-253.
227. Wu C., Wais M., Sheppy E., del Campo M., Zhang L. A glue-based, screw-free method for implantation of intra-cranial electrodes in young mice. J Neurosci Methods 2008, 171:126-131.
228. Xiong Y., Mahmood A., Chopp M. Animal models of traumatic brain injury. Nat Rev Neurosci 2013, 14(2):128-142.
229. Xu J., Fan Y., Li L., Qiu Y., Wang Z., Han S., et al. Hyperthermia-induced seizures: development of hyperthermia-prone and hyperthermia-resistant rats. Epilepsy Res 2013, 106(3):311-317.
230. Yang J., Woodhall G.L., Jones R.S.G. Tonic facilitation of glutamate release by presynaptic NR2B-containing NMDA receptors is increased in the entorhinal cortex of chronically epileptic rats. J Neurosci 2006, 26:406-410.
231. Yin P., Li Z., Wang Y.-Y., Qiao N.-N., Huang S.-Y., Sun R.-P., et al. Neonatal immune challenge exacerbates seizure-induced hippocampus-dependent memory impairment in adult rats. Epilepsy Behav 2013, 27:9-17.
232. Young D., Lawlor P.a., Leone P., Dragunow M., During M.J. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med 1999, 5(4):448-453.
233. Young G.B., Blume W.T. Painful epileptic seziures. Brain 1983, 106:537-554.
234. Zayachkivsky A., Lehmkuhle M.J., Fisher J.H., Ekstrand J.J., Dudek F.E. Recording EEG in immature rats with a novel miniature telemetry system. J Neurophysiol 2013, 109:900-911.
235. Zhao Q., Holmes G.L. Repetitive seizures in the immature brain. Models of seizures and epilepsy 2005, 341-350. Academic Press, Waltham. A. Pitkänen, P.A. Schwartzkroin, S.L. Moshé (Eds.).