Sensitive and critical periods in the development of handling induced seizures in mice lacking synapsins: Differences between synapsin I and synapsin II knockouts

Experimental Neurology

Volumn 247, Issue , 2013, Pages 59-65

  Etholm, Lars ^a,b   Bahonjic, Elma ^b   Heggelund, Paul ^b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Environmental factors; Epilepsy; Handling induced seizures; Plasticity; Synaptic transmission

Indexed keywords

SYNAPSIN I; SYNAPSIN II;

ANIMAL CARE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; GENE INACTIVATION; GENOTYPE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEIZURE; SYNAPSIN I GENE; SYNAPSIN II GENE; TONIC CLONIC SEIZURE;

ENVIRONMENTAL FACTORS; EPILEPSY; HANDLING-INDUCED SEIZURES; PLASTICITY; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; CHI-SQUARE DISTRIBUTION; CRITICAL PERIOD (PSYCHOLOGY); DISEASE MODELS, ANIMAL; DRUGS, CHINESE HERBAL; HANDLING (PSYCHOLOGY); MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SEIZURES; SYNAPSINS;

EID: 84876974787     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.03.025     Document Type: Article

References (52)

1. Andersen S.L., Teicher M.H. Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci. 2008, 31:183-191.
2. Baldelli P., Fassio A., Valtorta F., Benfenati F. Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J. Neurosci. 2007, 27:13520-13531.
3. Ben-Ari Y., Tremblay E., Riche D., Ghilini G., Naquet R. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 1981, 6:1361-1391.
4. Bischof H.J. Behavioral and neuronal aspects of developmental sensitive periods. Neuroreport 2007, 18:461-465.
5. Bogen I.L., Boulland J.L., Mariussen E., Wright M.S., Fonnum F., Kao H.T., Walaas S.I. Absence of synapsin I and II is accompanied by decreases in vesicular transport of specific neurotransmitters. J. Neurochem. 2006, 96:1458-1466.
6. Bogen I.L., Jensen V., Hvalby O., Walaas S.I. Synapsin-dependent development of glutamatergic synaptic vesicles and presynaptic plasticity in postnatal mouse brain. Neuroscience 2009, 158:231-241.
7. Boido D., Farisello P., Cesca F., Ferrea E., Valtorta F., Benfenati F., Baldelli P. Cortico-hippocampal hyperexcitability in synapsin I/II/III knockout mice: age-dependency and response to the antiepileptic drug levetiracetam. Neuroscience 2010, 171:268-283.
8. Bond T.L., Drage M., Heinrichs S.C. Seizure-prone EL mice exhibit deficits in pup nursing and retrieval assessed using a novel method of maternal behavior phenotyping. Epilepsy Behav. 2003, 4:57-64.
9. Cesca F., Baldelli P., Valtorta F., Benfenati F. The synapsins: key actors of synapse function and plasticity. Prog. Neurobiol. 2010, 91:313-348.
10. Chiappalone M., Casagrande S., Tedesco M., Valtorta F., Baldelli P., Martinoia S., Benfenati F. Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks. Cereb. Cortex 2009, 19:1422-1439.
11. Chin L.S., Li L., Ferreira A., Kosik K.S., Greengard P. Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9230-9234.
12. Corradi A., Zanardi A., Giacomini C., Onofri F., Valtorta F., Zoli M., Benfenati F. Synapsin-I- and synapsin-II-null mice display an increased age-dependent cognitive impairment. J. Cell Sci. 2008, 121:3042-3051.
13. Dews P.B., Wiesel T.N. Consequences of monocular deprivation on visual behaviour in kittens. J. Physiol. 1970, 206:437-455.
14. Etholm L., Heggelund P. Seizure elements and seizure element transitions during tonic-clonic seizure activity in the synapsin I/II double knockout mouse: a neuroethological description. Epilepsy Behav. 2009, 14:582-590.
15. Etholm L., Arabadzisz D., Lipp H.P., Heggelund P. Seizure logging: a new approach to synchronized cable-free EEG and video recordings of seizure activity in mice. J. Neurosci. Methods 2010, 192:254-260.
16. Etholm L., Bahonjic E., Walaas S.I., Kao H.T., Heggelund P. Neuroethologically delineated differences in the seizure behavior of synapsin 1 and synapsin 2 knock-out mice. Epilepsy Res. 2012, 99:252-259.
17. Farisello P., Boido D., Nieus T., Medrihan L., Cesca F., Valtorta F., Baldelli P., Benfenati F. Synaptic and extrasynaptic origin of the excitation/inhibition imbalance in the hippocampus of synapsin I/II/III knockout mice. Cereb. Cortex 2012.
18. Feng J., Chi P., Blanpied T.A., Xu Y., Magarinos A.M., Ferreira A., Takahashi R.H., Kao H.T., McEwen B.S., Ryan T.A., Augustine G.J., Greengard P. Regulation of neurotransmitter release by synapsin III. J. Neurosci. 2002, 22:4372-4380.
19. Ferreira A., Kosik K.S., Greengard P., Han H.Q. Aberrant neurites and synaptic vesicle protein deficiency in synapsin II-depleted neurons. Science 1994, 264:977-979.
20. Ferreira A., Chin L.S., Li L., Lanier L.M., Kosik K.S., Greengard P. Distinct roles of synapsin I and synapsin II during neuronal development. Mol. Med. 1998, 4:22-28.
21. Frankel W.N. Genetics of complex neurological disease: challenges and opportunities for modeling epilepsy in mice and rats. Trends Genet. 2009, 25:361-367.
22. Gitler D., Takagishi Y., Feng J., Ren Y., Rodriguiz R.M., Wetsel W.C., Greengard P., Augustine G.J. Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J. Neurosci. 2004, 24:11368-11380.
23. Gitler D., Cheng Q., Greengard P., Augustine G.J. Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles. J. Neurosci. 2008, 28:10835-10843.
24. Goddard G.V., McIntyre D.C., Leech C.K. A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol. 1969, 25:295-330.
25. Gordon J.A., Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 1996, 16:3274-3286.
26. Heinrichs S.C. Neurobehavioral consequences of stressor exposure in rodent models of epilepsy. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:808-815.
27. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005, 6:877-888.
28. Ishida N., Kasamo K., Nakamoto Y., Suzuki J. Epileptic seizure of El mouse initiates at the parietal cortex: depth EEG observation in freely moving condition using buffer amplifier. Brain Res. 1993, 608:52-57.
29. Ketzef M., Kahn J., Weissberg I., Becker A.J., Friedman A., Gitler D. Compensatory network alterations upon onset of epilepsy in synapsin triple knock-out mice. Neuroscience 2011, 189:108-122.
30. Kielland A., Erisir A., Walaas S.I., Heggelund P. Synapsin utilization differs among functional classes of synapses on thalamocortical cells. J. Neurosci. 2006, 26:5786-5793.
31. Knudsen E.I. Instructed learning in the auditory localization pathway of the barn owl. Nature 2002, 417:322-328.
32. Knudsen E.I. Sensitive periods in the development of the brain and behavior. J. Cogn. Neurosci. 2004, 16:1412-1425.
33. Korbey S.M., Heinrichs S.C., Leussis M.P. Seizure susceptibility and locus ceruleus activation are reduced following environmental enrichment in an animal model of epilepsy. Epilepsy Behav. 2008, 12:30-38.
34. Leussis M.P., Heinrichs S.C. Routine tail suspension husbandry facilitates onset of seizure susceptibility in EL mice. Epilepsia 2006, 47:801-804.
35. Leussis M.P., Heinrichs S.C. Temporal ontogeny of circuit activation prior to the onset of seizure susceptibility in EL/Suz mice. Neuroscience 2007, 145:33-41.
36. Mandell J.W., Townes-Anderson E., Czernik A.J., Cameron R., Greengard P., De C.P. Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 1990, 5:19-33.
37. Mandell J.W., Czernik A.J., De C.P., Greengard P., Townes-Anderson E. Differential expression of synapsins I and II among rat retinal synapses. J. Neurosci. 1992, 12:1736-1749.
38. McIntyre D.C., Gilby K.L. Mapping seizure pathways in the temporal lobe. Epilepsia 2008, 49(Suppl. 3):23-30.
39. Mutoh K., Ito M., Tsuda H., Shiraishi H., Oguro K., Shirasaka Y., Okuno T., Mikawa H. Depth EEG in mutant epileptic E1 mice: demonstration of secondary generalization of the seizure from the hippocampus. Electroencephalogr. Clin. Neurophysiol. 1993, 86:205-212.
40. Owe S.G., Erisir A., Heggelund P. Terminals of the major thalamic input to visual cortex are devoid of synapsin proteins. Neuroscience 2013, (E-pub ahead of print) (in press). 10.1016/j.neuroscience.2013.03.031.
41. Panayiotopoulos C.P., Obeid T., Tahan A.R. Juvenile myoclonic epilepsy: a 5-year prospective study. Epilepsia 1994, 35:285-296.
42. Pohl M., Mares P. Effects of flunarizine on metrazol-induced seizures in developing rats. Epilepsy Res. 1987, 1:302-305.
43. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1972, 32:281-294.
44. Rosahl T.W., Geppert M., Spillane D., Herz J., Hammer R.E., Malenka R.C., Sudhof T.C. Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell 1993, 75:661-670.
45. Rosahl T.W., Spillane D., Missler M., Herz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., Südhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 1995, 375:488-493.
46. Silva A.J., Rosahl T.W., Chapman P.F., Marowitz Z., Friedman E., Frankland P.W., Cestari V., Cioffi D., Sudhof T.C., Bourtchuladze R. Impaired learning in mice with abnormal short-lived plasticity. Curr. Biol. 1996, 6:1509-1518.
47. Suzuki J. Investigations of epilepsy with a mutant animal (EL mouse) model. Epilepsia 2004, 45(Suppl. 8):2-5.
48. Terada S., Tsujimoto T., Takei Y., Takahashi T., Hirokawa N. Impairment of inhibitory synaptic transmission in mice lacking synapsin I. J. Cell Biol. 1999, 145:1039-1048.
49. Todorova M.T., Burwell T.J., Seyfried T.N. Environmental risk factors for multifactorial epilepsy in EL mice. Epilepsia 1999, 40:1697-1707.
50. Turski W.A., Cavalheiro E.A., Bortolotto Z.A., Mello L.M., Schwarz M., Turski L. Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis. Brain Res. 1984, 321:237-253.
51. Veliskova J., Velisek L., Mares P., Rokyta R. Ketamine suppresses both bicuculline- and picrotoxin-induced generalized tonic-clonic seizures during ontogenesis. Pharmacol. Biochem. Behav. 1990, 37:667-674.
52. Wiesel T.N., Hubel D.H. Single-Cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 1963, 26:1003-1017.