Selective changes in inhibition as determinants for limited hyperexcitability in the insular cortex of epileptic rats

European Journal of Neuroscience

Volumn 31, Issue 11, 2010, Pages 2014-2023

  Bortel, Aleksandra ^a   Longo, Daniela ^b   De Guzman, Philip ^a   Dubeau, François ^a   Biagini, Giuseppe ^b   Avoli, Massimo ^a,c  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Interneuron; Neuropeptide Y; Parvalbumin; Pilocarpine; Temporal lobe epilepsy

Indexed keywords

NEUROPEPTIDE Y; PARVALBUMIN; PILOCARPINE; 4 AMINOBUTYRIC ACID; MUSCARINIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; EPILEPSY; EXCITATORY POSTSYNAPTIC POTENTIAL; INSULA; MALE; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; ACTION POTENTIAL; ANATOMY AND HISTOLOGY; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; ELECTROPHYSIOLOGY; HUMAN; INTERNEURON; METABOLISM; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION; TEMPORAL LOBE; TEMPORAL LOBE EPILEPSY;

ACTION POTENTIALS; ANIMALS; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; EPILEPSY, TEMPORAL LOBE; GAMMA-AMINOBUTYRIC ACID; HUMANS; INTERNEURONS; MALE; MUSCARINIC AGONISTS; NEURAL INHIBITION; NEUROPEPTIDE Y; PARVALBUMINS; PILOCARPINE; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION; TEMPORAL LOBE;

EID: 77953195143     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07225.x     Document Type: Article

References (47)

1. Allen, G.V., Saper, C.B., Hurley, K.M. Cechetto, D.F. (1991) Organization of visceral and limbic connections in the insular cortex of the rat. J. Comp. Neurol., 311, 1 16.
2. André, V., Marescaux, C., Nehlig, A. Fritschy, J.M. (2001) Alterations of hippocampal GABAergic system contribute to development of spontaneous recurrent seizures in the rat lithium-pilocarpine model of temporal lobe epilepsy. Hippocampus, 11, 452 468.
3. Augustine, J.R. (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Rev., 22, 229 244.
4. Barba, C., Barbati, G., Minotti, L., Hoffmann, D. Kahane, P. (2007) Ictal clinical and scalp-EEG findings differentiating temporal lobe epilepsies from temporal 'plus' epilepsies. Brain, 130, 1957 1967.
5. Benini, R. Avoli, M. (2006) Altered inhibition in lateral amygdala networks in a rat model of temporal lobe epilepsy. J. Neurophysiol., 95, 2143 2154.
6. Bernhardt, B.C., Worsley, K.J., Kim, H., Evans, A.C., Bernasconi, A. Bernasconi, N. (2009) Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy. Neurology, 72, 1747 1754.
7. Biagini, G., Merlo Pich, E., Carani, C., Marrama, P., Gustafsson, J.A., Fuxe, K. Agnati, L.F. (1993) Indole-pyruvic acid, a tryptophan ketoanalogue, antagonizes the endocrine but not the behavioral effects of repeated stress in a model of depression. Biol. Psychiatry, 33, 712 719.
8. Biagini, G., Sala, D. Zini, I. (1995) Diethyldithiocarbamate, a superoxide dismutase inhibitor, counteracts the maturation of ischemic-like lesions caused by endothelin-1 intrastriatal injection. Neurosci. Lett., 190, 212 216.
9. Biagini, G., D'Arcangelo, G., Baldelli, E., D'Antuono, M., Tancredi, V. Avoli, M. (2005) Impaired activation of CA3 pyramidal neurons in the epileptic hippocampus. Neuromolecular Med., 7, 325 342.
10. Biagini, G., Baldelli, E., Longo, D., Contri, M.B., Guerrini, U., Sironi, L., Gelosa, P., Zini, I., Ragsdale, D.S. Avoli, M. (2008) Proepileptic influence of a focal vascular lesion affecting entorhinal cortex-CA3 connections after status epilepticus. J. Neuropathol. Exp. Neurol., 67, 687 701.
11. Blaesse, P., Airaksinen, M.S., Rivera, C. Kaila, K. (2009) Cation-chloride cotransporters and neuronal function. Neuron, 61, 820 838.
12. Bouilleret, V., Dupont, S., Spelle, L., Baulac, M., Samson, Y. Semah, F. (2002) Insular cortex involvement in mesiotemporal lobe epilepsy: a positron emission tomography study. Ann. Neurol., 51, 202 208.
13. Brenner, R., Chen, Q.H., Vilaythong, A., Toney, G.M., Noebels, J.L. Aldrich, R.W. (2005) BK channel beta4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nat. Neurosci., 8, 1752 1759.
14. Butcher, K.S. Cechetto, D.F. (1995) Autonomic responses of the insular cortex in hypertensive and normotensive rats. Am. J. Physiol., 268, 214 222.
15. Cats, E.A., Kho, K.H., Van Nieuwenhuizen, O., Van Veelen, C.W., Gosselaar, P.H. Van Rijen, P.C. (2007) Seizure freedom after functional hemispherectomy and a possible role for the insular cortex: the Dutch experience. J. Neurosurg., 107, 275 280.
16. Cavalheiro, E.A., Leite, J.P., Bortolotto, Z.A., Turski, W.A., Ikonomidou, C. Turski, L. (1991) Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia, 32, 778 782.
17. Cechetto, D.F. Saper, C.B. (1987) Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J. Comp. Neurol., 262, 27 45.
18. Curia, G., Longo, D., Biagini, G., Jones, R.S. Avoli, M. (2008) The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods, 172, 143 157.
19. Du, F., Eid, T., Lothman, E.W., Köhler, C. Schwarcz, R. (1995) Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J. Neurosci., 15, 6301 6313.
20. Gnatkovsky, V. de Curtis, M. (2006) Hippocampus-mediated activation of superficial and deep layer neurons in the medial entorhinal cortex of the isolated guinea pig brain. J. Neurosci., 26, 873 881.
21. Guenot, M. Isnard, J. (2008) Epilepsy and insula. Neurochirurgie, 54, 374 381.
22. de Guzman, P., Inaba, Y., Biagini, G., Baldelli, E., Mollinari, C., Merlo, D. Avoli, M. (2006) Subiculum network excitability is increased in a rodent model of temporal lobe epilepsy. Hippocampus, 16, 843 860.
23. de Guzman, P., Inaba, Y., Baldelli, E., de Curtis, M., Biagini, G. Avoli, M. (2008) Network hyperexcitability within the deep layers of the pilocarpine-treated rat entorhinal cortex. J. Physiol., 586, 1867 1883.
24. Huberfeld, G., Wittner, L., Clemenceau, S., Baulac, M., Kaila, K., Miles, R. Rivera, C. (2007) Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J. Neurosci., 27, 9866 9873.
25. Inaba, Y., de Guzman, P. Avoli, M. (2006) NMDA receptor-mediated transmission contributes to network 'hyperexcitability' in the rat insular cortex. Eur. J. Neurosci., 23, 1071 1076.
26. Isnard, J., Guénot, M., Ostrowsky, K., Sindou, M. Mauguière, F. (2000) The role of the insular cortex in temporal lobe epilepsy. Ann. Neurol., 48, 614 623.
27. Isnard, J., Guénot, M., Sindou, M. Mauguière, F. (2004) Clinical manifestations of insular lobe seizures: a stereo- electroencephalographic study. Epilepsia, 45, 1079 1090.
28. Jasmin, L., Rabkin, S.D., Granato, A., Boudah, A. Ohara, P.T. (2003) Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature, 424, 316 320.
29. Jasmin, L., Burkey, A.R., Granato, A. Ohara, P.T. (2004) Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J. Comp. Neurol., 468, 425 440.
30. - extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J. Neurophysiol., 93, 2117 2126.
31. Kelly, M.E., Staines, W.A. McIntyre, D.C. (2002) Secondary generalization of hippocampal kindled seizures in rats: examining the role of the piriform cortex. Brain Res., 957, 152 161.
32. Kodama, M., Yamada, N., Sato, K., Sato, T., Morimoto, K. Kuroda, S. (2001) The insular but not the perirhinal cortex is involved in the expression of fully-kindled amygdaloid seizures in rats. Epilepsy Res., 46, 169 178.
33. McIntyre, D.C. Gilby, K.L. (2008) Mapping seizure pathways in the temporal lobe. Epilepsia, 49, 23 30.
34. Merlo Pich, E., Messori, B., Zoli, M., Ferraguti, F., Marrama, P., Biagini, G., Fuxe, K. Agnati, L.F. (1992) Feeding and drinking responses to neuropeptide Y injections in the paraventricular hypothalamic nucleus of aged rats. Brain Res., 575, 265 271.
35. Mohapel, P., Zhang, X., Gillespie, G.W., Chlan-Fourney, J., Hannesson, D.K., Corley, S.M., Li, X.M. Corcoran, M.E. (2001) Kindling of claustrum and insular cortex: comparison to perirhinal cortex in the rat. Eur. J. Neurosci., 13, 1501 1519.
36. Oppenheimer, S.M., Wilson, J.X., Guiraudon, C. Cechetto, D.F. (1991) Insular cortex stimulation produces lethal cardiac arrhythmias: a mechanism of sudden death? Brain Res., 550, 115 121.
37. Pathak, H.R., Weissinger, F., Terunuma, M., Carlson, G.C., Hsu, F.C., Moss, S.J. Coulter, D.A. (2007) Disrupted dentate granule cell chloride regulation enhances synaptic excitability during development of temporal lobe epilepsy. J. Neurosci., 27, 14012 14022.
38. Paxinos, G. Watson, C. (2007) The rat brain in stereotaxic coordinates, 6th Edn. Elsevier Academic Press
39. Priel, M.R., dos Santos, N.F. Cavalheiro, E.A. (1996) Developmental aspects of the pilocarpine model of epilepsy. Epilepsy Res., 26, 115 121.
40. Racine, R.J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol., 32, 281 294.
41. Rosenblum, K., Berman, D.E., Hazvi, S., Lamprecht, R. Dudai, Y. (1997) NMDA receptor and the tyrosine phosphorylation of its 2B subunit in taste learning in the rat insular cortex. J. Neurosci., 17, 5129 5135.
42. Ryvlin, P., Rheims, S. Risse, G. (2006) Nocturnal frontal lobe epilepsy. Epilepsia, 47, 83 86.
43. Selke, K., Müller, A., Kukley, M., Schramm, J. Dietrich, D. (2006) Firing pattern and calbindin-D28k content of human epileptic granule cells. Brain Res., 1120, 191 201.
44. Shi, C.J. Cassell, M.D. (1998) Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J. Comp. Neurol., 399, 440 468.
45. Verma-Ahuja, S., Evans, M.S. Pencek, T.L. (1995) Evidence for decreased calcium dependent potassium conductance in hippocampal CA3 neurons of genetically epilepsy-prone rats. Epilepsy Res., 22, 137 144.
46. van Vliet, E.A., Aronica, E., Tolner, E.A., Lopes da Silva, F.H. Gorter, J.A. (2004) Progression of temporal lobe epilepsy in the rat is associated with immunocytochemical changes in inhibitory interneurons in specific regions of the hippocampal formation. Exp. Neurol., 187, 367 379.
47. Williams, S., Vachon, P. Lacaille, J.C. (1993) Monosynaptic GABA-mediated inhibitory postsynaptic potentials in CA1 pyramidal cells of hyperexcitable hippocampal slices from kainic acid-treated rats. Neuroscience, 52, 541 554.