Developmental emergence of transient and persistent hippocampal events and oscillations and their association with infant seizure susceptibility

European Journal of Neuroscience

Volumn 26, Issue 10, 2007, Pages 2719-2730

  Mohns, Ethan J ^a   Karlsson, Karl Æ ^b   Blumberg, Mark S ^a  

^a E11 SSH   (United States)

^b REYKJAVIK UNIVERSITY   (Iceland)

Author keywords

Fast oscillations; Gamma; Interictal; Rat; Ripple; Sharp waves

Indexed keywords

KAINIC ACID;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRODE; ELECTROENCEPHALOGRAM; HIPPOCAMPUS; IN VIVO STUDY; MALE; NERVE EXCITABILITY; NEUROPHYSIOLOGY; NONHUMAN; OSCILLATION; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; SEIZURE; SPIKE WAVE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CORTICAL SYNCHRONIZATION; DISEASE SUSCEPTIBILITY; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; HIPPOCAMPUS; KAINIC ACID; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; SPECTRUM ANALYSIS;

EID: 36148982665     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05928.x     Document Type: Article

References (70)

1. Andersen, P., Bliss, T.V.P. Skrede, K.K. (1971) Unit analysis of hippocampal population spikes. Exp. Brain Res., 13, 208 221.
2. Baram, T.Z., Gerth, A. Schultz, L. (1997) Febrile seizures: an appropriate-aged model suitable for long-term studies. Brain Res. Dev. Brain Research, 98, 265 270.
3. Bragin, A., Azizyan, A., Almajano, J., Wilson, C.L. Engel, J. Jr. (2005) Analysis of chronic seizure onsets after intrahippocampal kainic acid injection in freely moving rats. Epilepsia, 46, 1592 1598.
4. Bragin, A., Engel, J. Jr., Wilson, C.L., Fried, I. Mathern, G.W. (1999a) Hippocampal and entorhinal cortex high-frequency oscillations (100-500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia, 40, 127 137.
5. Bragin, A., Engel, J. Jr., Wilson, C.L., Vizentin, E. Mathern, G.W. (1999b) Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia, 40, 1210 1221.
6. Bragin, A., Jandó, G., Nádasdy, Z., van Landeghem, M. Buzsaki, G. (1995) Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J. Neurophysiol., 73, 1691 1705.
7. Bragin, A., Mody, I., Wilson, C.L. Engel, J. Jr. (2002) Local generation of fast ripples in epileptic brain. J. Neurosci., 22, 2012 2021.
8. Bragin, A., Wilson, C.L., Almajano, J., Mody, I. Engel, J. Jr. (2004) High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia, 45, 1017 1023.
9. Buhl, D.L. Buzsaki, G. (2005) Developmental emergence of hippocampal fast-field 'ripple' oscillations in the behaving rat pups. Neuroscience, 134, 1423 1430.
10. Buzsaki, G. (1984) Long-term changes of hippocampal sharp-waves following high frequency afferent activation. Brain Res., 300, 179 182.
11. Buzsaki, G. (1986) Hippocampal sharp waves: Their origin and significance. Brain Res., 398, 242 252.
12. Buzsaki, G. (1989) Two-stage model of memory trace formation: a role for 'noisy' brain states. Neuroscience, 31, 551 570.
13. Buzsáki, G. (2002) Theta oscillations in the hippocampus. Neuron, 33, 325 340.
14. Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J. Wise, K. (1992) High-frequency network oscillation in the hippocampus. Science, 256, 1025 1027.
15. Buzsaki, G., Hsu, M., Slamka, C., Gage, F.H. Horvath, Z. (1991) Emergence and propagation of interictal spikes in the subcortically denervated hippocampus. Hippocampus, 1, 163 180.
16. Buzsaki, G., Leung, L.W. Vanderwolf, C.H. (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res. Rev., 287, 139 171.
17. Buzsaki, G., Ponomareff, G.L., Bayardo, F., Ruiz, R. Gage, F.H. (1989) Neuronal activity in the subcortically denervated hippocampus: a chronic model for epilepsy. Neuroscience, 28, 527 538.
18. Chrobak, J.J. Buzsaki, G. (1994) Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J. Neurosci., 14, 6160 6170.
19. Corner, M.A. Kwee, P. (1976) Cyclic EEG and motility patterns during sleep in restrained infant rats. Electroencephalogr. Clin. Neurophysiol., 41, 64 72.
20. Csicsvari, J., Jamieson, B., Wise, K.D. Buzsaki, G. (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron, 37, 311 322.
21. Fisahn, A., Pike, F.G., Buhl, E.H. Paulsen, O. (1998) Cholinergic induction of network oscillations at 40 HZ. in the hippocampus in vitro. Nature, 394, 186 189.
22. Fiumelli, H. Woodin, M.A. (2007) Role of activity-dependent regulation of neuronal chloride homeostasis in development. Curr. Opin. Neurobiol., 17, 81 86.
23. Ganguly, K., Schinder, A.F., Wong, S.T. Poo, M. (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell, 105, 521 532.
24. Gomez-Di Cesare, C.M., Smith, K.L., Rice, F.L. Swann, J.W. (1997) Axonal remodeling during postnatal maturation of CA3 hippocampal pyramidal neurons. J. Comp. Neurol., 384, 165 180.
25. Gramsbergen, A., Schwartze, P. Prechtl, H.F.R. (1970) The postnatal development of behavioral states in the rat. Dev. Psychobiol., 3, 267 280.
26. Hauser, W.A. (1995) Epidemiology of epilepsy in children. Neurosurgery Clinics North Am., 6, 419 429.
27. Holmes, G.L. Ben-Ari, Y. (1998) Seizures in the developing brain: perhaps not so benign after all. Neuron, 21, 1231 1234.
28. Jensen, F.E. (1999) Acute and chronic effects of seizures in the developing brain: experimental models. Epilepsia, 40 (Suppl. 1 S51 S58.
29. Jensen, F.E. (2002) The role of glutamate receptor maturation in perinatal seizures and brain injury. Int. J. Dev. Neuroscience, 20, 339 347.
30. Jensen, F.E., Applegate, C.D., Holtzman, D., Belin, T.R. Burchfiel, J.L. (1991) Epileptogenic effect of hypoxia in the immature rodent brain. Ann. Neurol., 29, 629 637.
31. Karlsson, K.Æ. Blumberg, M.S. (2002) The union of the state: Myoclonic twitching is coupled with nuchal muscle atonia in infant rats. Behav. Neuroscience, 116, 912 917.
32. Karlsson, K.Æ. Blumberg, M.S. (2003) Hippocampal theta in the newborn rat is revealed under conditions that promote REM sleep. J. Neuroscience, 23, 1114 1118.
33. Karlsson, K.Æ. Blumberg, M.S. (2004) Temperature-induced reciprocal activation of infant hippocampal field activity. J. Neurophysiol., 91, 583 588.
34. Karlsson, K.Æ., Gall, A.J., Mohns, E.J., Seelke, A.M.H. Blumberg, M.S. (2005) The neural substrates of infant sleep in rats. PLoS Biol., 3, 891 901.
35. Karlsson, K.Æ., Mohns, E.J., Viana Di Prisco, G. Blumberg, M.S. (2006) On the co-occurrence of startles and hippocampal sharp waves in newborn rats. Hippocampus, 16, 959 965.
36. Khalilov, I., Dzhala, V., Medina, I., Leinekugel, X., Melyan, Z., Lamsa, K., Khazipov, R. Ben-Ari, Y. (1999) Maturation of kainate-induced epileptiform activities in interconnected intact neonatal limbic structures in vitro. Eur. J. Neurosci., 11, 3468 3480.
37. Khalilov, I., Holmes, G.L. Ben-Ari, Y. (2003) In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat. Neurosci., 6, 1079 1085.
38. Khalilov, I., Le Van Quyen, M., Gozlan, H. Ben-Ari, Y. (2005) Epileptogenic actions of GABA and fast oscillations in the developing hippocampus. Neuron, 48, 787 796.
39. Khazipov, R., Khalilov, I., Tyzio, R., Morozova, E., Ben-Ari, Y. Holmes, G.L. (2004) Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur. J. Neurosci., 19, 590 600.
40. Kloosterman, F., van Haeften, T. Lopes da Silva, F.H. (2004) Two reentrant pathways in the hippocampal-entorhinal system. Hippocampus, 14, 1026 1039.
41. Lahtinen, H., Palva, J.M., Sumanen, S., Voipio, J., Kaila, K. Taira, T. (2001) Postnatal development of rat hippocampal gamma rhythm in vivo. J. Neurophysiol., 88, 1469 1474.
42. Le Van Quyen, M., Khalilov, I. Ben-Ari, Y. (2006) The dark side of high-frequency oscillations in the developing brain. Trends Neurosci., 29, 419 427.
43. Leblanc, M.O. Bland, B.H. (1979) Developmental aspects of hippocampal electrical activity and motor behavior in the rat. Exp. Neurol., 66, 220 237.
44. Leinekugel, X., Khazipov, R., Cannon, R., Hirase, H., Ben-Ari, Y. Buzsáki, G. (2002) Correlated bursts of activity in neonatal hippocampus in vivo. Science, 296, 2049 2052.
45. Leung, L.W. (1990) Spontaneous hippocampal interictal spikes following local kindling: time-course of change and relation to behavioral seizures. Brain Res., 513, 308 314.
46. Leung, L.S., Roth, L. Canning, K.J. (1995) Entorhinal inputs to hippocampal CA1 and dentate gyrus in the rat: a current-source-density study. J. Neurophysiol., 73, 2392 2403.
47. Mann, E.O., Suckling, J.M., Hajos, N., Greenfield, S.A. Paulsen, O. (2005) Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron, 45, 105 117.
48. Meaney, M.J. (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neuroscience, 24, 1161 1192.
49. Mitzdorf, U. (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev., 65, 37 100.
50. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. Seeburg, P.H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 12, 529 540.
51. Moshe, S.L. (1987) Epileptogenesis and the immature brain. Epilepsia, 28 (Suppl. 1 S3 S15.
52. Nicholson, C. Freeman, J.A. (1975) Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J. Neurophysiol., 38, 356 368.
53. O'Keefe, J. Nadel, L. (1978) The Hippocampus as a Cognitive Map. Clarendon Press, Oxford.
54. Penttonen, M., Kamondi, A., Acsady, L. Buzsaki, G. (1998) Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur. J. Neurosci., 10, 718 728.
55. Ritter, L.M., Vazquez, D.M. Meador-Woodruff, J.H. (2002) Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res. Dev. Brain Research, 139, 227 236.
56. Rivera, C., Voipio, J., Payne, J.A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., Pirvola, U., Saarma, M. Kaila, K. (1999) The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature, 397, 251 255.
57. Rozental, R., Srinivas, M., Gokhan, S., Urban, M., Dermietzel, R., Kessler, J.A., Spray, D.C. Mehler, M.F. (2000) Temporal expression of neuronal connexins during hippocampal ontogeny. Brain Res. Brain Res. Rev., 32, 57 71.
58. Sanchez, R.M. Jensen, F.E. (2001) Maturational aspects of epilepsy mechanisms and consequences for the immature brain. Epilepsia, 42, 577 585.
59. Schuchmann, S., Schmitz, D., Rivera, C., Vanhatalo, S., Salmen, B., Mackie, K., Sipila, S.T., Voipio, J. Kaila, K. (2006) Experimental febrile seizures are precipitated by a hyperthermia-induced respiratory alkalosis. Nat. Med., 12, 817 823.
60. Suzuki, S.S. Smith, G.K. (1987) Spontaneous EEG spikes in the normal hippocampus. I. Behavioral correlates, laminar profiles and bilateral synchrony. Electroencephalogr. Clin. Neurophysiol., 67, 348 359.
61. Suzuki, S.S. Smith, G.K. (1988) Spontaneous EEG spikes in the normal hippocampus. II. Relations to synchronous burst discharges. Electroencephalogr. Clin. Neurophysiol., 69, 532 540.
62. Swann, J.W. (1995) Synaptogenesis and epileptogenesis in developing cortical networks. In Schwartzkroin, P.A., Moshe, S.L., Noebels, J.L. Swann, J.W. (eds), Brain Development and Epilepsy. Oxford University Press, New York, pp. 195 233.
63. Swann, J.W. (2004) The effects of seizures on the connectivity and circuitry of the developing brain. Mental Retardation Dev. Disabilities Res. Rev., 10, 96 100.
64. Traub, R.D., Whittington, M.A., Colling, S.B., Buzsaki, G. Jefferys, J.G. (1996) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. (Lond.), 493, 471 484.
65. Velasco, A.L., Wilson, C.L., Babb, T.L. Engel, J. Jr. (2000) Functional and anatomic correlates of two frequently observed temporal lobe seizure-onset patterns. Neural Plasticity, 7, 49 63.
66. Vogt, A., Hormuzdi, S.G. Monyer, H. (2005) Pannexin1 and Pannexin2 expression in the developing and mature rat brain. Brain Res. Mol. Brain Research, 141, 113 120.
67. Wadman, W.J., Da Silva, F.H. Leung, L.W. (1983) Two types of interictal transients of reversed polarity in rat hippocampus during kindling. Electroencephalogr. Clin. Neurophysiol., 55, 314 319.
68. Winson, J. (1974) Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr. Clin. Neurophysiol., 36, 291 301.
69. - uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. (Lond.), 557, 829 841.
70. Ylinen, A., Bragin, A., Nádasdy, Z., Jandó, G., Szabó, I., Sik, A. Buzsáki, G. (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: Network and intracellular mechanisms. J. Neurosci., 15, 30 46.