Focal Scn1a knockdown induces cognitive impairment without seizures

Neurobiology of Disease

Volumn 54, Issue , 2013, Pages 297-307

  Bender, Alex C ^a   Natola, Heather ^a   Ndong, Christian ^a   Holmes, Gregory L ^a   Scott, Rod C ^a,b   Lenck Santini, Pierre Pascal ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Alzheimer's disease; Cognition; Dravet syndrome; Epilepsy; Medial septum; Nav1.1; Oscillations; Scn1a; Sodium channel

Indexed keywords

SMALL INTERFERING RNA; SODIUM CHANNEL NAV1.1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DIAGONAL BAND OF BROCA; DOWN REGULATION; FOREBRAIN; GENE SILENCING; HIPPOCAMPUS; LEARNING; MEMORY; MEMORY DISORDER; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEIZURE; SEPTUM PELLUCIDUM; SPATIAL MEMORY;

ANIMALS; BLOTTING, WESTERN; COGNITION DISORDERS; ELECTROENCEPHALOGRAPHY; EPILEPSIES, MYOCLONIC; GENE KNOCKDOWN TECHNIQUES; IMMUNOHISTOCHEMISTRY; MALE; NAV1.1 VOLTAGE-GATED SODIUM CHANNEL; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SEIZURES;

EID: 84876317530     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.12.021     Document Type: Article

References (58)

1. Akiyama M., Kobayashi K., Yoshinaga H., Ohtsuka Y. A long-term follow-up study of Dravet syndrome up to adulthood. Epilepsia 2010, 51:1043-1052.
2. Ben-ari Y., Holmes G.L. Effects of seizures on developmental processes in the immature brain. Lancet Neurol. 2006, 5:1055-1063.
3. Bender A.C., Morse R.P., Scott R.C., Holmes G.L., Lenck-Santini P.-P. SCN1A mutations in Dravet syndrome: impact of interneuron dysfunction on neural networks and cognitive outcome. Epilepsy Behav. 2012, 23:177-186.
4. Bland B.H., Oddie S.D. Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behav. Brain Res. 2001, 127:119-136.
5. Bragin A., Azizyan A., Almajano J., Engel J. The cause of the imbalance in the neuronal network leading to seizure activity can be predicted by the electrographic pattern of the seizure onset. J. Neurosci. 2009, 29:3660-3671.
6. Brazhnik E.S., Fox S.E. Action potentials and relations to the theta rhythm of medial septal neurons in vivo. Exp. Brain Res. 1999, 127:244-258.
7. Buzsaki G. Theta Oscillations in the Hippocampus. Neuron 2002, 33:325-340.
8. Cakir I., Perello M., Lansari O., Messier N.J., Vaslet C.A., Nillni E.A. Hypothalamic Sirt1 regulates food intake in a rodent model system. PLoS One 2009, 4:1-12.
9. Caraballo R.H., Fejerman N. Dravet syndrome: a study of 53 patients. Epilepsy Res. 2006, 70(Suppl. 1):S231-S238.
10. Catarino C.B., et al. Dravet syndrome as epileptic encephalopathy: evidence from long-term course and neuropathology. Brain 2011, 23:177-186.
11. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25.
12. Chauvière L., Rafrafi N., Thinus-Blanc C., Bartolomei F., Esclapez M., Bernard C. Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J. Neurosci. 2009, 29:5402-5410.
13. Colom L.V. Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease. J. Neurochem. 2006, 96:609-623.
14. Ennaceur A. Effects of lesions of the Substantia Innominata/Ventral Pallidum, globus pallidus and medial septum on rat's performance in object-recognition and radial-maze tasks: physostigmine and amphetamine treatments. Pharmacol. Res. 1998, 38:251-263.
15. Ennaceur A., Neave N., Aggleton J.P. Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav. Brain Res. 1996, 80:9-25.
16. Fischer Y. The hippocampal intrinsic network oscillator. J. Physiol. 2004, 554:156-174.
17. Givens B.S., Olton D.S. Cholinergic and GABAergic modulation of medial septal area: effect on working memory. Behav. Neurosci. 1990, 104:849-855.
18. Goutagny R., Jackson J., Williams S. Self-generated theta oscillations in the hippocampus. Nat. Neurosci. 2009, 12:1491-1493.
19. Guissouma H., Froidevaux M.-S.C., Hassani Z., Demeneix B.A. In vivo siRNA delivery to the mouse hypothalamus confirms distinct roles of TR beta isoforms in regulating TRH transcription. Neurosci. Lett. 2006, 406:240-243.
20. Hagan J.J., Verheijck E.E., Spigt M.H., Ruigt G.S. Behavioural and electrophysiological studies of entorhinal cortex lesions in the rat. Physiol. Behav. 1992, 51:255-266.
21. Hangya B., Borhegyi Z., Szilágyi N., Freund T.F., Varga V. GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J. Neurosci. 2009, 29:8094-8102.
22. Hassani Z., Lemkine G.F., Erbacher P., Palmier K., Alfama G., Giovannangeli C., Behr J.-P., Demeneix B.A. Lipid-mediated siRNA delivery down-regulates exogenous gene expression in the mouse brain at picomolar levels. J. Gene Med. 2005, 7:198-207.
23. Holmes G.L., Gairsa J.L., Chevassus-Au-Louis N., Ben-Ari Y. Consequences of neonatal seizures in the rat: morphological and behavioral effects. Ann. Neurol. 1998, 44:845-857.
24. Holmes G.L., Bender A.C., Wu E.X., Scott R.C., Lenck-Santini P.P., Morse R.P. Maturation of EEG oscillations in children with sodium channel mutations. Brain Dev. 2011, 34:469-477.
25. Huth T., Alzheimer C. Voltage-Dependent Na Channels as Targets of BACE1-Implications for Neuronal Firing and Beyond. Curr. Alzheimer Res. 2012, 9:184-188.
26. Kalume F., Yu F.H., Westenbroek R.E., Scheuer T., Catterall W.A. Reduced sodium current in Purkinje neurons from Nav1.1 mutant mice: implications for ataxia in severe myoclonic epilepsy in infancy. J. Neurosci. 2007, 27:11065-11074.
27. Kelsey J.E., Vargas H. Medial septal lesions disrupt spatial, but not nonspatial, working memory in rats. Behav. Neurosci. 1993, 107:565-574.
28. Khan O.I., Zhao Q., Miller F., Holmes G.L. Interictal spikes in developing rats cause long-standing cognitive deficits. Neurobiol. Dis. 2010, 39:362-371.
29. Kim D.Y., Carey B.W., Wang H., Ingano L.M., Binshtok A.M., Wertz M.H., Pettingell W.H., He P., Lee V.M.-Y., Woolf C.J., Kovacs D.M. BACE1 regulates voltage-gated sodium channels and neuronal activity. Nat. Cell Biol. 2007, 9:755-764.
30. Kovacs D.M., Gersbacher M.T., Kim D.Y. Alzheimer's secretases regulate voltage-gated sodium channels. Neurosci. Lett. 2010, 486:68-72.
31. Kumar P., Lee S.K., Shankar P., Manjunath N. A single siRNA suppresses fatal encephalitis induced by two different flaviviruses. PLoS Med. 2006, 3:505-514.
32. Martin M.S., Dutt K., Papale L.A., Dubé C.M., Dutton S.B., de Haan G., Shankar A., Tufik S., Meisler M.H., Baram T.Z., Goldin A.L., Escayg A. Altered function of the SCN1A voltage-gated sodium channel leads to gamma-aminobutyric acid-ergic (GABAergic) interneuron abnormalities. J. Biol. Chem. 2010, 285:9823-9834.
33. McCormick D., Contreras D. On the cellular and network bases of epileptic seizures. Annu. Rev. Physiol. 2001, 63:815-846.
34. McFarland W.L., Teitelbaum H., Hedges E.K. Relationship between hippocampal theta activity and running speed in the rat. J. Comp. Physiol. Psychol. 1975, 88:324-328.
35. Mumby D.G. Perspectives on object-recognition memory following hippocampal damage: lessons from studies in rats. Behav. Brain Res. 2001, 127:159-181.
36. Mumby D.G., Pinel J.P. Rhinal cortex lesions and object recognition in rats. Behav. Neurosci. 1994, 108:11-18.
37. O'Roak B.J., Deriziotis P., Lee C., Vives L., Schwartz J.J., Girirajan S., Karakoc E., MacKenzie A.P., Ng S.B., Baker C., Rieder M.J., Nickerson D.A., Bernier R., Fisher S.E., Shendure J., Eichler E.E. Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat. Genet. 2011, 43:585-589.
38. O'Roak B.J., et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 2012, 485:246-252.
39. Oakley J.C., Kalume F., Yu F.H., Scheuer T., Catterall W.A. Temperature- and age-dependent seizures in a mouse model of severe myoclonic epilepsy in infancy. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3994-3999.
40. Ohtsuka Y., Maniwa S., Ogino T., Yamatogi Y., Ohtahara S. Severe Myoclonic Epilepsy in Infancy: A Long-Term Follow-Up Study. Jpn. J. Psychiatry Neurol. 1991, 45:416-418.
41. Paxinos G., Watson C. The Rat Brain In stereotaxic Coordinates 2005, Elsevier Academic Press, Amsterdam; Boston; London. 5th ed.
42. Ragona F., Brazzo D., De Giorgi I., Morbi M., Freri E., Teutonico F., Gennaro E., Zara F., Binelli S., Veggiotti P., Granata T. Dravet syndrome: early clinical manifestations and cognitive outcome in 37 Italian patients. Brain Dev. 2010, 32:71-77.
43. Rawlins J., Feldon J., Gray J. Septo-hippocampal Connections and the Hippocampal Theta Rhythm. Exp. Brain Res. 1979, 37:49-63.
44. Sławińska U., Kasicki S. The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion. Brain Res. 1998, 796:327-331.
45. Stewart M., Fox S.E. Two populations of rhythmically bursting neurons in rat medial septum are revealed by atropine. J. Neurophysiol. 1989, 61:982-993.
46. Tang B., Dutt K., Papale L., Rusconi R., Shankar A., Hunter J., Tufik S., Yu F.H., Catterall W.A., Mantegazza M., Goldin A.L., Escayg A. A BAC transgenic mouse model reveals neuron subtype-specific effects of a Generalized Epilepsy with Febrile Seizures Plus (GEFS+) mutation. Neurobiol. Dis. 2009, 35:91-102.
47. Thinus-Blanc C., Save E., Poucet B., Buhot M. The effects of reversible inactivations of the hippocampus on exploratory activity and spatial memory. Hippocampus 1991, 1:365-372.
48. Varga V., Hangya B., Kránitz K., Ludányi A., Zemankovics R., Katona I., Shigemoto R., Freund T.F., Borhegyi Z. The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J. Physiol. 2008, 586:3893-3915.
49. Verret L., Mann E.O.O.O., Hang G.B., Barth A., Cobos I., Ho K., Devidze N., Masliah E., Kreitzer A., Mody I., Mucke L., Palop J.J. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012, 149:708-721.
50. Warburton E.C., Brown M.W. Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia 2010, 48:2262-2272.
51. Warburton E.C., Baird A.L., Morgan A., Muir J.L., Aggleton J.P. Disconnecting hippocampal projections to the anterior thalamus produces deficits on tests of spatial memory in rats. Eur. J. Neurosci. 2000, 12:1714-1726.
52. Weiss L.A., Escayg A., Kearney J.A., Trudeau M., MacDonald B.T., Mori M., Reichert J., Buxbaum J.D., Meisler M.H. Sodium channels SCN1A, SCN2A and SCN3A in familial autism. Mol. Psychiatry 2003, 8:186-194.
53. Wills T.J., Cacucci F., Burgess N., O'Keefe J. Development of the Hippocampal Cognitive Map in Preweanling Rats. Science 2010, 328:1573-1576.
54. Winson J. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 1978, 201:160-163.
55. Winters B.D., Forwood S.E., Cowell R.A., Saksida L.M., Bussey T.J. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J. Neurosci. 2004, 24:5901-5908.
56. Wolff M., Cassé-Perrot C., Dravet C. Severe myoclonic epilepsy of infants (Dravet syndrome): natural history and neuropsychological findings. Epilepsia 2006, 47(Suppl. 2):45-48.
57. Yu F.H., Mantegazza M., Westenbroek R.E., Robbins C.A., Kalume F., Burton K.A., Spain W.J., McKnight G.S., Scheuer T., Catterall W.A. Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat. Neurosci. 2006, 9:1142-1149.
58. Zuberi S.M., Brunklaus A., Birch R., Reavey E., Duncan J., Forbes G.H. Genotype-phenotype associations in SCN1A-related epilepsies. Neurology 2011, 76:594-600.