Aberrant neuronal responsiveness in the genetically epilepsy-prone rat: Acoustic responses and influences of the central nucleus upon the external nucleus of inferior colliculus

Brain Research

Volumn 761, Issue 2, 1997, Pages 263-270

  Chakravarty, D N ^a,b   Faingold, C L ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Audiogenic seizures; Genetically epilepsy prone rats; Inferior colliculus; Neuronal network; Seizures

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID;

ACOUSTICS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ELECTROSTIMULATION THERAPY; EPILEPSY; INFERIOR COLLICULUS; NERVE CELL; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; STEREOTAXIS; STIMULUS RESPONSE;

ACOUSTIC STIMULATION; ANIMALS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; EPILEPSY; EXCITATORY AMINO ACID AGONISTS; INFERIOR COLLICULUS; MICROINJECTIONS; N-METHYLASPARTATE; NEURONS; RATS; RATS, MUTANT STRAINS; RATS, SPRAGUE-DAWLEY; STIMULATION, CHEMICAL;

EID: 0030787936     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(97)00331-4     Document Type: Article

References (71)

1. L. Aitkin, The Auditory Midbrain. Structure and Function in the Central Auditory Pathway, Humana Press, Clifton, NJ, 1986, 246 pp.
2. C. Bernard, H.V. Wheal, Plasticity of AMPA and NMDA receptor-mediated epileptiform activity in a chronic model of temporal lobe epilepsy, Epilepsy Res. 21 (1995) 95-107.
3. R.A. Browning, Anatomy of generalized convulsive seizures, in: A. Malafosse, P. Genton, E. Hirsch, C. Marescaux, D. Broglin and R. Bernasconi (Eds.), Idiopathic Generalized Epilepsies: Clinical, Experimental and Genetic Aspects, John Libbey, London, 1994, pp. 399-413.
4. J.F. Brugge, C.D. Geisler, Auditory mechanisms of the lower brainstem, Annu. Rev. Neurosci. 1 (1978) 363-394.
5. A. Caicedo, H. Herbert, Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat, J. Comp. Neurol. 328 (1993) 377-392.
6. D.M. Caspary, A. Raza, B.A. Lawhorn Armour, J. Pippin, S.P. Arneric, Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus: Implications for neural presbycusis, J. Neuroscience 10 (1990) 2363-2372.
7. D.M. Caspary, R.H. Helfert, Two populations of commissural projections connecting like regions of the inferior colliculus immunostain for different amino acid transmitters, Soc. Neurosci. Abstr. 19 (1993) 1425.
8. D.N. Chakravarty, C.L. Faingold, Increased responsiveness and failure of habituation in neurons of the external nucleus of inferior colliculus associated with audiogenic seizures of the genetically epilepsy-prone rat, Exp. Neurol. 141 (1996) 280-286.
9. D.N. Chakravarty, C.L. Faingold, W.J. Terry, D.K. Naritoku, Audiogenic seizures in the genetically epilepsy-prone rat induce c-fos expression in the inferior colliculus and periaqueductal gray, Soc. Neurosci. Abstr. 19 (1993) 605.
10. A.G. Chapman, C.L. Faingold, G.P. Hart, H.M. Bowker, B.S. Meldrum, Brain regional amino acid levels in seizure susceptible rats: Changes related to sound-induced seizures, Neurochem. Int. 8 (1986) 273-279.
11. Q.X. Chen, R.K.S. Wong, Suppression of GABA-A receptor responses by NMDA application in hippocampal neurones acutely isolated from the adult guinea-pig, J. Physiol. 482 (1995) 353-362.
12. J.R. Coleman, W.J. Clerici, Sources of projections to subdivisions of the inferior colliculus in the rat, J. Comp. Neurol. 262 (1987) 215-226.
13. R.J. Cowie, G. Holstege, Dorsal mesencephalic projections to pons, medulla and spinal cord in the cat: limbic and non-limbic components, J. Comp. Neurol. 319 (1992) 536-559.
14. E. Covey, J.A. Kauer, J.H. Casseday, Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats, J. Neurosci. 16 (1996) 3009-3018.
15. M.C. Doretto, R.L. Burger, P.K. Mishra, N. Garcia-Cairasco, J.W. Dailey, P.C. Jobe, A microdialysis study of amino acid concentrations in the extracellular fluid of the substantia nigra of freely behaving GEPR-9s: Relationship to seizure predisposition, Epilepsy Res. 17 (1994) 157-165.
16. F.E. Dudek, J.P. Wuarin, J.G. Tasker, Y.I. Kim, W.J. Peacock, Neurophysiology of neocortical slices resected from children undergoing surgical treatment for epilepsy, J. Neurosci. Methods 59 (1995) 49-58.
17. M.J. During, J.S. Craig, T.D. Hernandez, G.M. Anderson, D.W. Gallager, Effect of amygdala kindling on the in vivo release of GABA and 5-HT in the dorsal raphe nucleus in freely moving rats, Brain Res. 584 (1992) 36-44.
18. M.S. Evans, K.E. Viola-McCabe, D.M. Caspary, C.L. Faingold, Loss of synaptic inhibition during repetitive stimulation in genetically epilepsy-prone rats (GEPR), Epilepsy Res. 18 (1994) 97-105.
19. C.L. Faingold, M.A. Travis, G. Gehlbach, W.E. Hoffmann, P.C. Jobe, H.E. Laird II, D.M. Caspary, Neuronal response abnormalities in the inferior colliculus of the genetically epilepsy-prone rat, Electroenceph. Clin. Neurophysiol. 63 (1986) 296-305.
20. C.L. Faingold, G. Gehlbach, D.M. Caspary, Decreased effectiveness of GABA-mediated inhibition in the inferior colliculus of the genetically epilepsy-prone rat, Exp. Neurol. 93 (1986) 145-159.
21. C.L. Faingold, M.H. Millan, C.A. Boersma, B.S. Meldrum, Excitant amino acids and audiogenic seizures in the genetically epilepsy-prone rat. I. Afferent seizure initiation pathway, Exp. Neurol. 99 (1988) 678-686.
22. C.L. Faingold, W.E. Hoffmann, D.M. Caspary, Effects of excitant amino acids on acoustic responses of inferior colliculus neurons, Hearing Res. 40 (1989) 127-136.
23. C.L. Faingold, M.H. Millan, C.A. Boersma Anderson, B.S. Meldrum, Induction of audiogenic seizures in normal and genetically epilepsy-prone rats following focal microinjection of an excitant amino acid into reticular formation and auditory nuclei, Epilepsy Res. 3 (1989) 199-205.
24. C.L. Faingold, G. Gehlbach, D.M. Caspary, On the role of GABA as an inhibitory neurotransmitter in inferior colliculus neurons: Iontophoretic studies, Brain Res. 500 (1989) 302-312.
25. C.L. Faingold, C.A. Boersma Anderson, D.M. Caspary, Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons, Hearing Res. 52 (1991) 201-216.
26. C.L. Faingold, C.A. Boersma Anderson, Loss of intensity-induced inhibition in inferior colliculus neurons leads to audiogenic seizure susceptibility in behaving genetically epilepsy-prone rats, Exp. Neurol. 113 (1991) 354-363.
27. C.L. Faingold, D.K. Naritoku, The genetically epilepsy-prone rat: Neuronal networks and actions of amino acid neurotransmitters, in: C.L. Faingold, G.H. Fromm (Eds.), Drugs for Control of Epilepsy: Actions on Neuronal Networks Involved in Seizure Disorders, CRC Press, Boca Raton, FL, 1992, pp. 277-308.
28. C.L. Faingold, D.K. Naritoku, C.A. Copley, M.E. Randall, A. Riaz, C.A. Boersma Anderson, S.P. Arneric, Glutamate in the inferior colliculus plays a critical role in audiogenic seizure initiation, Epilepsy Res. 13 (1992) 95-105.
29. C.L. Faingold, M.E. Randall, D.K. Naritoku, C.A. Boersma Anderson, Noncompetitive and competitive NMDA antagonists exert anticonvulsant effects by actions on different sites within the neuronal network for audiogenic seizures, Exp. Neurol. 119 (1993) 198-204.
30. C.L. Faingold, M.J. Marcinczyk, D.J. Casebeer, M.E. Randall, S.P. Arneric, R.A. Browning, GABA in the inferior colliculus plays a critical role in control of audiogenic seizures, Brain Res. 640 (1994) 40-47.
31. C.L. Faingold, M.E. Randall, Pontine reticular formation neurons exhibit a premature and precipitous increase in acoustic responses prior to audiogenic seizures in genetically epilepsy-prone rats, Brain Res. 704 (1995) 218-226.
32. H. Faye-Lund, K. Osen, Anatomy of the inferior colliculus in rat, Anat. Embryol. 171 (1985) 1-20.
33. D.E. Feldman, E.I. Knudsen, NMDA and non-NMDA glutamate receptors in auditory transmission in the barn owl inferior colliculus, J. Neurosci. 14 (1994) 5939-5958.
34. M. Feliciano, S.J. Potashner, Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus, J. Neurochem. 65 (1995) 1348-1357.
35. E.M. Gould, C.R. Craig, W.W. Fleming, D.A. Taylor, Sensitivity of cerebellar purkinje neurons to neurotransmitters in genetically epileptic rats, J. Pharmacol. Exp. Ther. 259 (1991) 1008-1012.
36. A receptors in the subsensitivity of Purkinje neurons to GABA in genetic epilepsy prone rats, Brain Res. 698 (1995) 62-68.
37. 3H]glutamate-binding sites in rat central nervous system, J. Neurosci. 4 (1984) 2133-2144.
38. R.F. Huffman, O.W. Henson Jr., The descending auditory pathway and acousticomotor systems: Connections with the inferior colliculus, Brain Res. Rev. 15 (1990) 295-323.
39. A receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus, J. Neurophysiol. 75 (1996) 1901-1908.
40. P.C. Jobe, P.K. Mishra, J.W. Dailey, Genetically epilepsy-prone rats: actions of antiepileptic drugs and monoaminergic neurotransmitters, in: C.L. Faingold, G.H. Fromm (Eds.), Drugs for Control of Epilepsy: Actions on Neuronal Networks Involved in Seizure Disorders, CRC Press, Boca Raton, FL, 1992, pp. 253-275.
41. T. Kaneko, K. Itoh, R. Shigemoto, N. Mizuno, Glutaminase-like immunoreactivity in the lower brainstem and cerebellum of the adult rat, Neurosci. 32 (1989) 79-98.
42. J. Kapur, E.W. Lothman, NMDA receptor activation mediates the loss of GABAergic inhibition induced by recurrent seizures, Epilepsy Res. 5 (1990) 103-111.
43. S. Kaura, H.F. Bradford, A.M.J. Young, M.J. Croucher, P.D. Hughes, Effect of amygdaloid kindling on the content and release of amino acids from the amygdaloid complex: in vivo and in vitro studies, J. Neurochem. 65 (1995) 1240-1249.
44. E.I. Knudsen, M. Konishi, A neural map of auditory space in the owl, Science 200 (1978) 795-797.
45. S.M. Lasley, Q. Yan, Diminished potassium-stimulated GABA release in vivo in genetically epilepsy-prone rats, Neurosci. Lett. 175 (1994) 145-148.
46. F.E.N. Le Beau, A. Rees, M.S. Malmierca, Contribution of GABA-and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus, J. Neurophysiol. 75 (1996) 902-919.
47. A. Lenmann, Abnormalities in the levels of extracellular and tissue amino acids in the brain of the seizure-susceptible rat, Epilepsy Res. 3 (1989) 130-137.
48. K. Matsuyama, Y. Kobayashi, K. Takakusaki, S. Mori, H. Kimura, Termination mode and branching patterns of reticuloreticular and reticulospinal fibers of the nucleus reticularis pontis oralis in the cat: An anterograde PHA-L tracing study, Neurosci. Res. 17 (1993) 9-21.
49. T.J. McCown, R.S. Greenwood, G.D. Frye, G.R. Breese, Electrically elicited seizures from the inferior colliculus: a potential site for the genesis of epilepsy, Exp. Neurol. 86 (1984) 527-542.
50. J.L. Meyerhoff, R.E. Carter, D.L. Yourick, B. Stauch Slusher, J.T. Coyle, Genetically epilepsy-prone rats have increased brain regional activity of an enzyme which liberates glutamate from N-acetylaspartyl-glutamate, Brain Res. 593 (1992) 140-143.
51. M.H. Millan, B.S. Meldrum, C.L. Faingold, Induction of audiogenic seizure susceptibility by focal infusion of excitant amino acid or bicuculline into the inferior colliculus of normal rats, Exp. Neurol. 91 (1986) 634-639.
52. M.H. Millan, B.S. Meldrum, C.A. Boersma, C.L. Faingold, Excitant amino acids and audiogenic seizures in the genetically epilepsy-prone rat. II. Efferent seizure propagating pathway, Exp. Neurol. 99 (1988) 687-698.
53. L.J. Mouton, G. Holstege, The periaqueductal gray in the cat projects to lamina VIII and the medial part of lamina VII throughout the length of the spinal cord, Exp. Brain Res. 101 (1994) 253-264.
54. A. Najlerahim, P.J. Harrison, A.J.L. Barton, J. Hefferman, R.C.A. Pearson, Distribution of messenger RNAs encoding the enzymes glutaminase, aspartate aminotransferase and glutamic acid decarboxylase in rat brain, Mol. Brain Res. 7 (1990) 317-333.
55. P. N'Gouemo, D.M. Caspary, C.L. Faingold, Decreased GABA effectiveness in the inferior colliculus neurons during ethanol withdrawal in rats susceptible to audiogenic seizures, Brain Res. 724 (1996) 200-204.
56. P. N'Gouemo, C.L. Faingold, Periaqueductal gray neurons exhibit increased responsiveness associated with audiogenic seizures in the genetically epilepsy-prone rat, Neuroscience (1997) in press.
57. D.L. Oliver, G.E. Beckius, A. Shneiderman, Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: a study using electron microscopic autoradiography, J. Comp. Neurol. 360 (1995) 17-32.
58. E. Olivier, T. Kitama, A. Grantyn, Anatomical evidence for ipsilateral collicular projections to the spinal cord in the cat, Exp. Brain Res. 100 (1994) 160-164.
59. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Coordinates, Academic Press, Orlando, FL, 1986.
60. M.E. Randall, C.L. Faingold, Aberrant neuronal firing patterns in deep layers of superior colliculus subserve audiogenic seizure expression in genetically epilepsy-prone rats, Soc. Neurosci. Abstr. 21 (1995) 1961.
61. C.E. Ribak, M.Y. Byun, G.T. Ruiz, R.J. Reiffenstein, Increased levels of amino acid neurotransmitters in the inferior colliculus of genetically epilepsy-prone rat, Epilepsy Res. 2 (1988) 9-13.
62. 67) mRNA, Epilepsy Res. 14 (1993) 105-113.
63. C.E. Ribak, V. Khurana, N.T. Lien, The effect of midbrain collicular knife cuts on audiogenic seizure severity in the genetically epilepsy-prone rat, J. Brain Res. 35 (1994) 303-311.
64. C.E. Ribak, C.L. Morin, The role of the inferior colliculus in a genetic model of audiogenic seizures, Anat. Embryol. 191 (1995) 279-295.
65. C.E. Ribak, W.M.Y. Tong, N.C. Brecha, Increased expression of GABA transporters in the inferior colliculus of genetically epilepsy-prone rats (GEPR-9s), Epilepsia 37 (1996) S4.
66. S. Simler, E. Hirsch, L. Danober, J. Motte, M. Vergnes, C. Marescaux, C-fos expression after single and kindled audiogenic seizures in Wistar rats, Neurosci. Lett. 175 (1994) 58-62.
67. P.H. Smith, Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique, J. Neurosci. 12 (1992) 3700-3715.
68. A.M. Snyder-Keller, M.G. Pierson, Audiogenic seizures induce c-fos in a model of developmental epilepsy, Neurosci. Lett. 135 (1992) 108-112.
69. A. Stelzer, H. Shi, Impairment of GABA-A receptor function by N-methyl-D-aspartate-mediated calcium influx in isolated CA1 pyramidal cells, Neuroscience 62 (1994) 813-828.
70. M. Vater, H. Habbicht, M. Kössl, B. Grothe, The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats, J. Comp. Physiol. 171 (1992) 541-553.
71. S. Verma-Ahuja, T.L. Pencek, Hippocampal CA1 neuronal properties in genetically epilepsy-prone rats: evidence for increased excitation, Epilepsy Res. 18 (1994) 205-215.