Reduced chemical and electrical connections of fast-spiking interneurons in experimental cortical dysplasia

Journal of Neurophysiology

Volumn 112, Issue 6, 2014, Pages 1277-1290

  Zhou, Fu Wen ^a   Roper, Steven N ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Epilepsy; Inhibition; Irradiation; Neocortex; Regular spiking

Indexed keywords

BIOCYTIN; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; CORTICAL DYSPLASIA; ELECTRIC CURRENT; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; IMMUNOREACTIVITY; INTERNEURON; MALE; NERVE ENDING; NERVE FIBER; NERVE POTENTIAL; NEUROPATHOLOGY; NEWBORN; NONHUMAN; POSTSYNAPTIC INHIBITION; PULSE WAVE; PYRAMIDAL NERVE CELL; RAT; RAT MODEL; SPIKE WAVE; STELLATE CELL; SYNAPTIC TRANSMISSION; TARGET CELL; ACTION POTENTIAL; ANIMAL; BRAIN CORTEX; ELECTRICAL SYNAPSE; INHIBITORY POSTSYNAPTIC POTENTIAL; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; ELECTRICAL SYNAPSES; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MALE; MALFORMATIONS OF CORTICAL DEVELOPMENT; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84907246301     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00126.2014     Document Type: Article

References (93)

1. Ali AB, Bannister AP, Thomson AM. Robust correlations between action potential duration and the properties of synaptic connections in layer 4 interneurones in neocortical slices from juvenile rats and adult rat and cat. J Physiol 580: 149–169, 2007.
2. Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, Connors BW, Golomb D. The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J Neurosci 22: 4142–4152, 2002.
3. Arion D, Horvath S, Lewis DA, Mirnics K. Infragranular gene expression disturbances in the prefrontal cortex in schizophrenia: signature of altered neural development? Neurobiol Dis 37: 738–746, 2010.
4. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8: 45–56, 2007.
5. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987–3000, 2003.
6. Blümcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, Becker A, Cepeda C, Cendes F, Colombo N, Crino P, Cross JH, Delalande O, Dubeau F, Duncan J, Guerrini R, Kahane P, Mathern G, Najm I, Ozkara C, Raybaud C, Represa A, Roper SN, Salamon N, Schulze-Bonhage A, Tassi L, Vezzani A, Spreafico R. The clinico-pathological spectrum of focal cortical dysplasias: a revised classification system of the International League Against Epilepsy. Epilepsia 52: 158–174, 2011.
7. Brill J, Huguenard JR. Enhanced infragranular and supragranular synaptic input onto layer 5 pyramidal neurons in a rat model of cortical dysplasia. Cereb Cortex 20: 2926–2938, 2010.
8. A receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4: 1166–1172, 1998.
9. Calcagnotto ME, Paredes MF, Tihan T, Barbaro NM, Baraban SC. Dysfunction of synaptic inhibition in epilepsy associated with focal cortical dysplasia. J Neurosci 25: 9649–9657, 2005.
10. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17: 3894–3906, 1997.
11. 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.
12. Connors BW. Electrical signaling with neuronal gap junctions. In: Connexins: a Guide, edited by Harris AL, Locke D. New York: Humana, 2009, p. 143–164.
13. Connors BW, Long MA. Electrical synapses in the mammalian cortex. Annu Rev Neurosci 27: 393–418, 2004.
14. Cossart R, Bernard C, Ben-Ari Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signaling in epilepsies. Trends Neurosci 28: 108–115, 2005.
15. Cowan D, Geller LM. Long-term pathological effects of prenatal X-irradiation on the central nervous system of the rat. J Neuropathol Exp Neurol 19: 488–527, 1960.
16. Crino PB, Duhaime AC, Baltuch G, White R. Differential expression of glutamate and GABA-A receptor subunit mRNA in cortical dysplasia. Neurology 56: 906–913, 2001.
17. Curley AA, Arion D, Volk DW, Asafu-Adjei JK, Sampson AR, Fish KN, Lewis DA. Cortical deficits of glutamic acid decarboxylase 67 expression in schizophrenia: Clinical, protein, and cell type-specific features. Am J Psychiatry 168: 921–929, 2011.
18. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31: 477–485, 2001.
19. DeFazio RA, Hablitz JJ. Reduction of zolpidem sensitivity in a freeze lesion model of neocortical dysgenesis. J Neurophysiol 81: 404–407, 1999.
20. DeFelipe J. Chandelier cells and epilepsy. Brain 122: 1807–1822, 1999.
21. DeFelipe J, López-Cruz PL, Benavides-Piccione R, Bielza C, Larrañaga P, Anderson S, Burkhalter A, Cauli B, Fairén A, Feldmeyer D, Fishell G, Fitzpatrick D, Freund TF, González-Burgos G, Hestrin S, Hill S, Hof PR, Huang J, Jones EG, Kawaguchi Y, Kisvárday Z, Kubota Y, Lewis DA, Marín O, Markram H, McBain CJ, Meyer HS, Monyer H, Nelson SB, Rockland K, Rossier J, Rubenstein JL, Rudy B, Scanziani M, Shepherd GM, Sherwood CC, Staiger JF, Tamás G, Thomson A, Wang Y, Yuste R, Ascoli GA. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14: 202–216, 2013.
22. Deukmedjian AJ, King MA, Cuda C, Roper SN. The GABAergic system of the developing neocortex has a reduced capacity to recover from in utero injury in experimental cortical dysplasia. J Neuropathol Exp Neurol 63: 1265–1273, 2004.
23. Draguhn A, Traub RD, Schmitz D, Jefferys JG. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394: 189–192, 1998.
24. Ferrer I, Oliver B, Russi A, Casas R, Rivera R. Parvalbumin and calbindin D28k immunocytochemistry in human neocortical epileptic foci. J Neurol Sci 123: 18–25, 1994.
25. Galarreta M, Hestrin S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1: 587–594, 1998.
26. Galarreta M, Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402: 72–75, 1999.
27. Galarreta M, Hestrin S. Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci USA 99: 12438–12443, 2002.
28. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75–79, 1999.
29. Gonchar Y, Burkhalter A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7: 347–358, 1997.
30. Hestrin S. The strength of electrical synapses. Science 334: 315–316, 2011.
31. Hestrin S, Galarreta M. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci 28: 304–309, 2005.
32. Holmgren C, Harkany T, Svennenfors B, Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551: 139–153, 2003.
33. Hormuzdi SG, Pais I, LeBeau FE, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31: 487–495, 2001.
34. Jacobs KM, Prince DA. Excitatory and inhibitory postsynaptic currents in a rat model of epileptogenic microgyria. J Neurophysiol 93: 687–696, 2005.
35. Kellinghaus C, Kunieda T, Ying Z, Pan A, Luders HO, Najm IM. Severity of histopathologic abnormalities and in vivo epileptogenicity in the in utero radiation model of rats is dose dependent. Epilepsia 45: 583–591, 2004.
36. Kondo S, Najm I, Kunieda T, Perryman S, Yacubova K, Luders HO. Electroencephalographic characterization of an adult rat model of radiation-induced cortical dysplasia. Epilepsia 42: 1221–1227, 2001.
37. Korman B, Krsek P, Duchowny M, Maton B, Pacheco-Jacome E, Rey G. Early seizure onset and dysplastic lesion extent independently disrupt cognitive networks. Neurology 81: 745–751, 2013.
38. Krsek P, Maton B, Korman B, Pacheco-Jacome E, Jayakar P, Dunoyer C, Rey G, Morrison G, Ragheb J, Vinters HV, Resnick T, Duchowny M. Different features of histopathological subtypes of pediatric focal cortical dysplasia. Ann Neurol 63: 758–769, 2008.
39. Krsek P, Pieper T, Karlmeier A, Hildebrandt M, Kolodziejczyk D, Winkler P, Pauli E, Blümcke I, Holthausen H. Different presurgical characteristics and seizure outcomes in children with focal cortical dysplasia type I or II. Epilepsia 50: 125–137, 2009.
40. LeBeau FE, Traub RD, Monyer H, Whittington MA, Buhl EH. The role of electrical signaling via gap junctions in the generation of fast network oscillations. Brain Res Bull 62: 3–13, 2003.
41. 2+ uptake into barrel cortex slices of spontaneously hypertensive rats. Metab Brain Dis 16: 133–141, 2001.
42. Leventer RJ, Phelan EM, Coleman LT, Kean MJ, Jackson GD, Harvey AS. Clinical and imaging features of cortical malformations in childhood. Neurology 53: 715–722, 1999.
43. Lim KC, Crino PB. Focal malformations of cortical development: new vistas for molecular pathogenesis. Neuroscience 252: 262–276, 2013.
44. Ma Y, Prince DA. Functional alterations in GABAergic fast-spiking interneurons in chronically injured epileptogenic neocortex. Neurobiol Dis 47: 102–113, 2012.
45. MacVicar BA, Dudek FE. Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213: 782–785, 1981.
46. Marín O. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 13: 107–120, 2012.
47. Marín-Padilla M, Tsai RJ, King MA, Roper SN. Altered corticogenesis and neuronal morphology in irradiation-induced cortical dysplasia: a Golgi-Cox study. J Neuropathol Exp Neurol 62: 1129–1143, 2003.
48. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500: 409–440, 1997.
49. Mattia D, Olivier A, Avoli M. Seizure-like discharges recorded in human dysplastic neocortex maintained in vitro. Neurology 45: 1391–1395, 1995.
50. McCormick DA, Connors BW, Lighthall JW, Prince DA. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782–806, 1985.
51. Oghlakian RO, Tilelli CQ, Hiremath GK, Alexopoulos AV, Najm IM. Single injection of a low dose of pentylenetetrazole leads to epileptogenesis in an animal model of cortical dysplasia. Epilepsia 50: 801–810, 2009.
52. Palmini A, Gambardella A, Andermann F, Dubeau F, da Costa JC, Olivier A, Tampieri D, Gloor P, Quesney F, Andermann E, Paglioli E, Paglioli-Neto E, Andermann LC, Leblanc R, Kim HI. Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol 37: 476–487, 1995.
53. Palmini A, Najm I, Avanzini G, Babb T, Guerrini R, Foldvary-Schaefer N, Jackson G, Lüders HO, Prayson R, Spreafico R, Vinters HV. Terminology and classification of the cortical dysplasias. Neurology 62: S2–S8, 2004.
54. Pangratz-Fuehrer S, Hestrin S. Synaptogenesis of electrical and GABAergic synapses of fast-spiking inhibitory neurons in the neocortex. J Neurosci 31: 10767–10775, 2011.
55. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic, 1986.
56. Perez Velazquez JL, Carlen PL. Gap junctions, synchrony and seizures. Trends Neurosci 23: 68–74, 2000.
57. A receptor subunits in widespread brain regions in the freeze-lesion model of focal cortical malformations. J Neurosci 20: 5045–5053, 2000.
58. Roper SN, Eisenschenk S, King MA. Reduced density of parvalbumin- and calbindin D28-immunoreactive neurons in experimental cortical dysplasia. Epilepsy Res 37: 63–71, 1999.
59. Roper SN, Gilmore RL, Houser CR. Experimentally induced disorders of neuronal migration produce an increased propensity for electrographic seizures in rats. Epilepsy Res 21: 205–219, 1995.
60. Roper SN, King MA, Abraham LA, Boillot MA. Disinhibited in vitro neocortical slices containing experimentally induced cortical dysplasia demonstrate hyperexcitability. Epilepsy Res 26: 443–449, 1997.
61. Rouach N, Avignone E, Même W, Koulakoff A, Venance L, Blomstrand F, Giaume C. Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell 94: 457–475, 2002.
62. Rubenstein JL. Annual research review: Development of the cerebral cortex: implications for neurodevelopmental disorders. J Child Psychol Psychiatry 52: 339–355, 2011.
63. Rubenstein JL, Merzenich MM. Model of autism: Increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255–267, 2003.
64. Schubert D, Kötter R, Zilles K, Luhmann HJ, Staiger JF. Cell type-specific circuits of cortical layer IV spiny neurons. J Neurosci 23: 2961–2970, 2003.
65. Selemon LD, Ceritoglu C, Tilak Ratnanather J, Wang L, Harms MP, Aldridge K, Begović A, Csernansky JG, Miller MI, Rakic P. Distinct abnormalities of the primate prefrontal cortex caused by ionizing radiation in early or midgestation. J Comp Neurol 521: 1040–1053, 2013.
66. Song S, Sjöström PJ, Reigl M, Nelson S, Chklovskii DB. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3: e68, 2005.
67. Spreafico R, Battaglia G, Arcelli P, Andermann F, Dubeau F, Palmini A, Olivier A, Villemure JG, Tampieri D, Avanzini G, Avoli M. Cortical dysplasia: an immunocytochemical study of three patients. Neurology 50: 27–36, 1998.
68. Staiger JF, Flagmeyer I, Schubert D, Zilles K, Kötter R, Luhmann HJ. Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cereb Cortex 14: 690–701, 2004.
69. Stevens CF, Wang Y. Facilitation and depression at single central synapses. Neuron 14: 795–802, 1995.
70. Sun QQ, Huguenard JR, Prince DA. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci 26: 1219–1230, 2006.
71. Tamás G, Somogyi P, Buhl EH. Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J Neurosci 18: 4255–4270, 1998.
72. Tarczy-Hornoch K, Martin KA, Jack JJ, Stratford KJ. Synaptic interactions between smooth and spiny neurones in layer 4 of cat visual cortex in vitro. J Physiol 508: 351–363, 1998.
73. Tassi L, Garbelli R, Colombo N, Bramerio M, Lo Russo G, Deleo F, Milesi G, Spreafico R. Type I focal cortical dysplasia: surgical outcome is related to histopathology. Epileptic Disord 12: 181–191, 2010.
74. Thomson AM, Lamy C. Functional maps of neocortical local circuitry. Front Neurosci 1: 19–42, 2007.
75. Thomson AM, West DC, Hahn J, Deuchars J. Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol 496: 81–102, 1996.
76. Thomson AM, West DC, Wang Y, Bannister AP. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2–5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labeling in vitro. Cereb Cortex 12: 936–953, 2002.
77. Traub RD, Pais I, Bibbig A, LeBeau FE, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA. Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc Natl Acad Sci USA 100: 1370–1374, 2003.
78. Volman V, Perc M, Bazhenov M. Gap junctions and epileptic seizures–two sides of the same coin? PLoS One 6: e20572, 2011.
79. Whittington MA, Traub RD. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26: 676–682, 2003.
80. Whittington MA, Traub RD, Jefferys JG. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612–615, 1995.
81. Woo NH, Lu B. Regulation of cortical interneurons by neurotrophins: from development to cognitive disorders. Neuroscientist 12: 43–56, 2006.
82. Woodruff AR, Sah P. Networks of parvalbumin-positive interneurons in the basolateral amygdala. J Neurosci 27: 553–563, 2007.
83. 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.
84. Xiang Z, Huguenard JR, Prince DA. Synaptic inhibition of pyramidal cells evoked by different interneuronal subtypes in layer v of rat visual cortex. J Neurophysiol 88: 740–750, 2002.
85. Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, Buzsáki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15: 30–46, 1995.
86. Zhou FW, Chen HX, Roper SN. Balance of inhibitory and excitatory synaptic activity is altered in fast-spiking interneurons in experimental cortical dysplasia. J Neurophysiol 102: 2514–2525, 2009.
87. Zhou FW, Jin Y, Matta SG, Xu M, Zhou FM. An ultra-short dopamine pathway regulates basal ganglia output. J Neurosci 29: 10424–10435, 2009.
88. Zhou FW, Matta SG, Zhou FM. Constitutively active TRPC3 channels regulate basal ganglia output neurons. J Neurosci 28: 473–482, 2008.
89. Zhou FW, Rani A, Martinez-Diaz H, Foster TC, Roper SN. Altered behavior in experimental cortical dysplasia. Epilepsia 52: 2293–2303, 2011.
90. Zhou FW, Roper SN. Densities of glutamatergic and GABAergic presynaptic terminals are altered in experimental cortical dysplasia. Epilepsia 51: 1468–1476, 2010.
91. Zhou FW, Roper SN. Altered firing rates and patterns in interneurons in experimental cortical dysplasia. Cereb Cortex 21: 1645–1658, 2011.
92. Zhou FW, Roper SN. Impaired hippocampal memory function and synaptic plasticity in experimental cortical dysplasia. Epilepsia 53: 850–859, 2012.
93. Zhu WJ, Roper SN. Reduced inhibition in an animal model of cortical dysplasia. J Neurosci 20: 8925–8931, 2000.