Inhibitory inputs to hippocampal interneurons are reorganized in Lis1 mutant mice

Journal of Neurophysiology

Volumn 102, Issue 2, 2009, Pages 648-658

  Jones, Daniel L ^a   Baraban, Scott C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID;

AGYRIA; ANIMAL TISSUE; ARTICLE; BRAIN MALFORMATION; CONTROLLED STUDY; EPILEPSY; GENE; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LIS1 GENE; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ACTION POTENTIALS; ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CLASSICAL LISSENCEPHALIES AND SUBCORTICAL BAND HETEROTOPIAS; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MEMBRANE POTENTIALS; MICE; MICE, MUTANT STRAINS; MICROTUBULE-ASSOCIATED PROTEINS; NEURAL PATHWAYS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; SOMATOSTATIN; TIME FACTORS;

EID: 68149158060     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00392.2009     Document Type: Article

References (60)

1. Ackman JB, Aniksztejn L, Crépel V, Becq H, Pellegrino C, Cardoso C, Ben-Ari Y, Represa A. Abnormal network activity in a targeted genetic model of human double cortex. J Neurosci 29: 313-327, 2009.
2. A receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4: 1166-1172, 1998.
3. Butt SJB, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48: 591-604, 2005.
4. Calcagnotto ME, Baraban SC. Prolonged NMDA-mediated responses, altered ifenprodil sensitivity, and epileptiform-like events in the malformed hippocampus of methylazoxymethanol exposed rats. J Neurophysiol 94: 153-162, 2005.
5. Calcagnotto ME, Paredes MF, Baraban SC. Heterotopic neurons with altered inhibitory synaptic function in an animal model of malformation- associated epilepsy. J Neurosci 22: 7596-7605, 2002.
6. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75-78, 1995.
7. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition, and epilepsy. Nat Neurosci 8: 1059-1068, 2005.
8. Cohen I, Huberfeld G, Miles R. Emergence of disinhibition-induced synchrony in the CA3 region of the guinea pig hippocampus in vitro. J Physiol 570: 583-594, 2006.
9. Cossart R, Bernard C, Ben-Ari Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci 28: 108-115, 2005.
10. Dudek FE, Hellier JL, Williams PA, Ferraro DJ, Staley KJ. The course of cellular alterations associated with the development of spontaneous seizures after status epilepticus. Prog Brain Res 135: 53-65, 2002.
11. Fleck MW, Hirotsune S, Gambello MJ, Phillips-Tansey E, Suares G, Mervis RF, Wynshaw-Boris A, McBain CJ. Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J Neurosci 20: 2439-2450, 2000.
12. Gant JC, Thibault O, Blalock EM, Yang J, Bachstetter A, Kotick J, Schauwecker PE, Hauser KF, Smith GM, Mervis R, Li Y, Barnes GN. Decreased number of interneurons and increased seizures in neuropilin 2 deficient mice: implications for autism and epilepsy. Epilepsia 50: 629-645, 2009.
13. Gavilán MP, Revilla E, Pintado C, Castaño A, Vizuete ML, Moreno-González I, Baglietto-Vargas D, Sánchez-Varo R, Vitorica J, Gutiérrez A, Ruano D. Molecular and cellular characterization of the age-related neuroinflammatory processes occurring in normal rat hippocampus: potential relation with the loss of somatostatin GABAergic neurons. J Neurochem 103: 984-996, 2007.
14. A receptor α1 subunit. J Neurophysiol 88: 3208-3217, 2002.
15. Guerrini R, Filippi T. Neuronal migration disorders, genetics, and epileptogenesis. J Child Neurol 20: 287-299, 2005.
16. Guerrini R, Marini C. Genetic malformations of cortical development. Exp Brain Res 173: 322-333, 2006.
17. Haas KZ, Sperber EF, Moshe SL, Stanton PK. Kainic acid-induced seizures enhance dentate gyrus inhibition by downregulation of GABA(B) receptors. J Neurosci 16: 4250-4260, 1996.
18. A receptor maturation in relation to eye opening in the rat visual cortex. Neuroscience 124: 161-171, 2004.
19. Hevner RF, Daza RA, Englund C, Kohtz J, Fink A. Postnatal shifts of interneuron position in the neocortex of normal and reeler mice: evidence for inward radial migration. Neuroscience 124: 605-618, 2004.
20. Holter NI, Zuber N, Bruehl C, Draguhn A. Functional maturation of developing interneurons in the molecular layer of mouse dentate gyrus. Brain Res 1186: 56-64, 2007.
21. Jacobs KM, Prince DA. Excitatory and inhibitory postsynaptic currents in a rat model of epileptogenic microgyria. J Neurophysiol 93: 687-696, 2005.
22. Jones DL, Baraban SC. Characterization of inhibitory circuits in the malformed hippocampus of Lis1 mutant mice. J Neurophysiol 98: 2737-2746, 2007.
23. Kato M, Dobyns WB. Lissencephaly and the molecular basis of neuronal migration. Hum Mol Genet 12: R89-R96, 2003.
24. Kerjan G, Koizumi H, Han EB, Dubé CM, Djakovic SN, Patrick GN, Baram TZ, Heinemann SF, Gleeson JG. Mice lacking doublecortin and doublecortin-like kinase 2 display altered hippocampal neuronal maturation and spontaneous seizures. Proc Natl Acad Sci USA 106: 6766-6771, 2009.
25. Klaassen A, Glykys J, Maguire J, Labarca C, Mody I, Boulter J. Seizures and enhanced cortical inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy. Proc Natl Acad Sci USA 103: 19152-19157, 2006.
26. Lacaille JC, Williams S. Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36: 349-359, 1990.
27. Liu Z, Steward R, Luo L. Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration, and axonal transport. Nat Cell Biol 2: 776-783, 2000.
28. Maas C, Tagnaouti N, Loebrich S, Behrend B, Lappe-Siefke C, Kneussel M. Neuronal cotransport of glycine receptor and the scaffold protein gephyrin. J Cell Biol 172: 441-451, 2006.
29. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004.
30. Massengill JL, Smith MA, Son DI, O'Dowd DK. Differential expression of K4-AP currents and Kv3.1 potassium channel transcripts in cortical neurons that develop distinct firing phenotypes. J Neurosci 17: 3136-3147, 1997.
31. McManus MF, Nasrallah IM, Pancoast MM, Wynshaw-Boris A, Golden JA. Lis1 is necessary for normal non-radial migration of inhibitory interneurons. Am J Pathol 165: 775-784, 2004.
32. Morin F, Beaulieu C, Lacaille JC. Cell-specific alterations in synaptic properties of hippocampal CA1 interneurons after kainite treatment. J Neurophysiol 80: 2836-2847, 1998.
33. Morin F, Beaulieu C, Lacaille JC. Alterations of perisomatic GABA synapses on hippocampal CA1 inhibitory interneurons and pyramidal cells in the kainate model of epilepsy. Neuroscience 93: 457-467, 1999.
34. Morozov YM, Freund TF. Postnatal development and migration of cholecystokinin-immunoreactive interneurons in rat hippocampus. Neuroscience 120: 923-939, 2003.
35. Morozov YM, Torii M, Rakic P. Origin, early commitment, migratory routes, and destination of cannabinoid type 1 receptor-containing interneurons. Cereb Cortex (April 3, 2009). doi:10.1093/cercor/bhp028.
36. Nusser Z, Cull-Candy S, Farrant M. Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude. Neuron 19: 697-709, 1997.
37. A receptor α subunits expression with the properties of IPSCs in the developing thalamus. J Neurosci 20: 2202-2208, 2000.
38. Okaty BW, Miller MN, Sugino K, Hempel CM, Nelson SB. Transcriptional and electrophysiological maturation of neocortical fast-spiking GABAergic interneurons. J Neurosci 29: 7040-7052, 2009.
39. Patel LS, Wenzel HJ, Schwartzkroin PA. Physiological and morphological characterization of dentate granule cells in the p35 knock-out mouse hippocampus: evidence for an epileptic circuit. J Neurosci 24: 9005-9014, 2004.
40. Paylor R, Hirotsune S, Gambello MJ, Yuva-Paylor L, Crawley JN, Wynshaw-Boris A. Impaired learning and motor behavior in heterozygous Pafah1b1 (Lis1) mutant mice. Learn Mem 6: 521-537, 1999.
41. A receptor subunits in seizure-prone and seizure-resistant rat models of temporal lobe epilepsy. J Neurosci 19: 4654-4661, 1999.
42. Rakic S, Yanagawa Y, Obata K, Faux C, Parnavelas JG, Nikolic M. Cortical interneurons require p35/Cdk5 for their migration and laminar organization. Cereb Cortex 19: 249-262, 2009.
43. A and glycine receptor-mediated synaptic currents in brain stem motoneurons. J Neurophysiol 90: 870-875, 2003.
44. Shao LR, Dudek FE. Changes in mIPSCs and sIPSCs after kainate treatment: evidence for loss of inhibitory input to dentate granule cells and possible compensatory responses. J Neurophysiol 94: 952-960, 2005.
45. Tanaka DH, Maekawa K, Yanagawa Y, Obata K, Murakami F. Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex. Development 133: 2167-2176, 2003.
46. Treiman DM. GABAergic mechanisms in epilepsy. Epilepsia 42, Suppl. 3: 8-12, 2001.
47. Trotter SA, Kapur J, Anzivino MJ, Lee KS. GABAergic synaptic inhibition is reduced before seizure onset in a genetic model of cortical malformation. J Neurosci 26: 10756-10767, 2006.
48. Tsai JW, Chen Y, Kriegstein AR, Vallee RB. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J Cell Biol 170: 935-945, 2005.
49. Uhlhaas PJ, Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52: 155-168, 2006.
50. Valdes-Sanchez L, Escamez T, Echevarria D, Ballesta JJ, Tabares-Seisdedos R, Reiner O, Martinez S, Geijo-Barrientos E. Postnatal alterations of the inhibitory synaptic responses recorded from cortical pyramidal neurons in the Lis1/sLis1 mutant mouse. Mol Cell Neurosci 35: 220-229, 2007.
51. Wang XJ, Buzsáki G. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16: 6402-6413, 1996.
52. Wang Y, Baraban SC. Granule cell dispersion and aberrant neurogenesis in the adult hippocampus of an LIS1 mutant mouse. Dev Neurosci 29: 91-98, 2007.
53. Wang Y, Baraban SC. Aberrant dentate gyrus cytoarchitecture and fiber lamination in Lis1 mutant mice. Hippocampus 18: 758-765, 2008.
54. Waterman-Storer CM, Karki SB, Kuznetsov SA, Tabb JS, Weiss DG, Langford GM, Holzbaur EL. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci USA 94: 12180-12185, 1997.
55. Wenzel HJ, Robbins CA, Tsai LH, Schwartzkroin PA. Abnormal morphological and functional organization of the hippocampus in a p35 mutant model of cortical dysplasia associated with spontaneous seizures. J Neurosci 21: 983-998, 2001.
56. Wenzel HJ, Woolley CS, Robbins CA, Schwartzkroin PA. Kainic acid-induced mossy fiber sprouting and synapse formation in the dentate gyrus of rats. Hippocampus 10: 244-260, 2000.
57. Williams PA, Hellier JL, White AM, Staley KJ, Dudek FE. Development of spontaneous seizures after experimental status epilepticus: implications for understanding epileptogenesis. Epilepsia 48, Suppl. 5: 157-163, 2007.
58. Wittner L, Eross L, Szabo Z, Toth SZ, Czirjak S, Halasz P, Freund TF, Magloczky ZS. Synaptic reorganization of calbindin-positive neurons in the human hippocampal CA1 region in temporal lobe epilepsy. Neuroscience 115: 961-978, 2002.
59. Xiang H, Chen HX, Yu XX, King MA, Roper SN. Reduced excitatory drive in interneurons in an animal model of cortical dysplasia. J Neurophysiol 96: 569-578, 2006.
60. Zsombok A, Jacobs KM. Postsynaptic currents prior to onset of epileptiform activity in rat microgyria. J Neurophysiol 98: 178-186, 2007.