Electrical induction of spikes in the hippocampus impairs recognition capacity and spatial memory in rats

Epilepsy and Behavior

Volumn 9, Issue 4, 2006, Pages 549-556

  Shatskikh, Tatiana N ^a   Raghavendra, Meghana ^a   Zhao, Qian ^a   Cui, Zhiyong ^a   Holmes, Gregory L ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Animal models; CA1; Hippocampus; Morris water maze; Object recognition task; Radial arm maze; Rat; Spikes

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR COMMISSURE; ARTICLE; CONTROLLED STUDY; ELECTRIC CURRENT; ELECTROENCEPHALOGRAM; EPILEPSY; EPILEPTIC DISCHARGE; HIPPOCAMPUS; MALE; MAZE TEST; MEMORY DISORDER; MICROELECTRODE; NONHUMAN; PATHOPHYSIOLOGY; RAT; SPATIAL DISCRIMINATION; SPATIAL MEMORY; SPIKE WAVE;

ANIMALS; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; HIPPOCAMPUS; MALE; MAZE LEARNING; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); SPATIAL BEHAVIOR;

EID: 33751313580     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2006.08.014     Document Type: Article

References (83)

1. Berger H. Über das Elektrenkephalogramm des Menschen [I. Mitteilung]. Arch Psychiatr 87 (1929) 527-570
2. Gibbs E.L., Lorimer F.M., and Gibbs F.A. Clinical correlates of exceedingly fast activity in the electroencephalogram. Dis Nerv Syst 11 11 (1950) 323-326
3. Dichter M., and Spencer W.A. Penicillin-induced interictal discharges from the cat hippocampus: I. Characteristics and topographical features. J Neurophysiol 32 (1969) 649-662
4. Prince D.A., and Connors B.W. Mechanisms of interictal epileptogenesis. Adv Neurol 44 (1986) 275-299
5. De Curtis M., and Avanzini G. Interictal spikes in focal epileptogenesis. Prog Neurobiol 63 (2001) 541-567
6. Engel Jr. J. A practical guide for routine EEG studies in epilepsy. J Clin Neurophysiol 1 (1984) 109-142
7. Blume W.T., and Kaibara M. Localization of epileptic foci in children. Can J Neurol Sci 18 4, Suppl. (1991) 570-572
8. Blume W.T. Pathogenesis of Lennox-Gastaut syndrome: considerations and hypotheses. Epileptic Disord 3 (2001) 183-196
9. Herzog A.G. A relationship between particular reproductive endocrine disorders and the laterality of epileptiform discharges in women with epilepsy. Neurology 43 (1993) 1907-1910
10. Herzog A.G., Drislane F.W., Schomer D.L., et al. Abnormal pulsatile secretion of luteinizing hormone in men with epilepsy: relationship to laterality and nature of paroxysmal discharges. Neurology 40 (1990) 1557-1561
11. Barbarosie M., and Avoli M. CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures. J Neurosci 17 (1997) 9308-9314
12. de Curtis M., Librizzi L., and Biella G. Discharge threshold is enhanced for several seconds after a single interictal spike in a model of focal epileptogenesis. Eur J Neurosci 14 (2001) 174-178
13. Staley K., Hellier J.L., and Dudek F.E. Do interictal spikes drive epileptogenesis?. Neuroscientist 11 (2005) 272-276
14. Holmes G.L., and Lenck-Santini P.P. Role of interictal epileptiform abnormalities in cognitive impairment. Epilepsy Behav 8 (2006) 504-515
15. Holmes G.L. Clinical evidence that epilepsy is a progressive disorder with special emphasis on epilepsy syndromes that do progress. Adv Neurol 97 (2006) 323-331
16. Nabbout R., and Dulac O. Epileptic encephalopathies: a brief overview. J Clin Neurophysiol 20 (2003) 393-397
17. Shields W.D. Catastrophic epilepsy in childhood. Epilepsia 41 Suppl. 2 (2000) S2-S6
18. Tuchman R.F., and Rapin I. Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates. Pediatrics 99 (1997) 560-566
19. Brinciotti M., Matricardi M., Paolella A., Porro G., and Benedetti P. Neuropsychological correlates of subclinical paroxysmal EEG activity in children with epilepsy: 1. Qualitative features (generalized and focal abnormalities). Funct Neurol 4 (1989) 235-239
20. Yan Liu X., and Wong V. Spectrum of epileptic syndromes with electrical status epilepticus during sleep in children. Pediatr Neurol 22 (2000) 371-379
21. De Negri M., Baglietto M.G., Battaglia F.M., Gaggero R., Pessagno A., and Recanati L. Treatment of electrical status epilepticus by short diazepam (DZP) cycles after DZP rectal bolus test. Brain Dev 17 (1995) 330-333
22. Deonna T., Davidoff V., Maeder-Ingvar M., Zesiger P., and Marcoz J.P. The spectrum of acquired cognitive disturbances in children with partial epilepsy and continuous spike-waves during sleep: a 4-year follow-up case study with prolonged reversible learning arrest and dysfluency. Eur J Paediatr Neurol 1 (1997) 19-29
23. Laporte N., Sebire G., Gillerot Y., Guerrini R., and Ghariani S. Cognitive epilepsy: ADHD related to focal EEG discharges. Pediatr Neurol 27 (2002) 307-311
24. Weglage J., Demsky A., Pietsch M., and Kurlemann G. Neuropsychological, intellectual, and behavioral findings in patients with centrotemporal spikes with and without seizures. Dev Med Child Neurol 39 (1997) 646-651
25. Deonna T., Zesiger P., Davidoff V., Maeder M., Mayor C., and Roulet E. Benign partial epilepsy of childhood: a longitudinal neuropsychological and EEG study of cognitive function. Dev Med Child Neurol 42 (2000) 595-603
26. Rapin I. Autistic regression and disintegrative disorder: how important the role of epilepsy?. Semin Pediatr Neurol 2 (1995) 278-285
27. Aldenkamp A.P., and Arends J. Effects of epileptiform EEG discharges on cognitive function: is the concept of "transient cognitive impairment" still valid?. Epilepsy Behav 5 Suppl. 1 (2004) S25-S34
28. Fonseca L.C., Tedrus G.M., Lalloni D.T., Tella L.M., Maluf P., and de Sousa V.D. Transient cognitive impairment during generalized or diffuse epileptiform EEG discharges. Arq Neuropsiquiatr 63 3B (2005) 817-824
29. Binnie C.D. Cognitive impairment during epileptiform discharges: is it ever justifiable to treat the EEG?. Lancet Neurol 2 (2003) 725-730
30. Stafstrom C.E., and Holmes G.L. Infantile spasms: criteria for an animal model. Int Rev Neurobiol 49 (2002) 391-411
31. Swanson L.W., Wyss J.M., and Cowan W.M. An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181 (1978) 681-715
32. Andersen P., Bliss T.V., Lomo T., Olsen L.I., and Skrede K.K. Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 76 (1969) 4-5 A
33. Laurberg S., and Sorensen K.E. Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3). Brain Res 212 (1981) 287-300
34. Bliss T.V., Lancaster B., and Wheal H.V. Long-term potentiation in commissural and Schaffer projections to hippocampal CA1 cells: an in vivo study in the rat. J Physiol 341 (1983) 617-626
35. Jarrard L.E. On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60 (1993) 9-26
36. Squire L.R., Stark C.E., and Clark R.E. The medial temporal lobe. Annu Rev Neurosci 27 (2004) 279-306
37. O'Keefe J. An allocentric spatial model for the hippocampal cognitive map. Hippocampus 1 (1991) 230-235
38. Morris R.G., Garrud P., Rawlins J.N., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297 (1982) 681-683
39. Eichenbaum H. The hippocampus and mechanisms of declarative memory. Behav Brain Res 103 (1999) 123-133
40. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11 (1984) 47-60
41. Hodges H. Maze procedures: the radial-arm and water maze compared. Brain Res Cogn Brain Res 3 (1996) 167-181
42. Spiers H.J., Burgess N., Maguire E.A., et al. Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. Brain 124 Pt. 12 (2001) 2476-2489
43. Jeltsch H., Bertrand F., Lazarus C., and Cassel J.C. Cognitive performances and locomotor activity following dentate granule cell damage in rats: role of lesion extent and type of memory tested. Neurobiol Learn Mem 76 (2001) 81-105
44. He J., Yamada K., Nakajima A., Kamei H., and Nabeshima T. Learning and memory in two different reward tasks in a radial arm maze in rats. Behav Brain Res 134 (2002) 139-148
45. Duva C.A., Floresco S.B., Wunderlich G.R., Lao T.L., Pinel J.P., and Phillips A.G. Disruption of spatial but not object-recognition memory by neurotoxic lesions of the dorsal hippocampus in rats. Behav Neurosci 111 (1997) 1184-1196
46. Forwood S.E., Winters B.D., and Bussey T.J. Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 15 (2005) 347-355
47. Mumby D.G. Perspectives on object-recognition memory following hippocampal damage: lessons from studies in rats. Behav Brain Res 127 (2001) 159-181
48. Wan H., Aggleton J.P., and Brown M.W. Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19 (1999) 1142-1148
49. Murray E.A., and Bussey T.J. Perceptual-mnemonic functions of the perirhinal cortex. Trends Cogn Sci 3 (1999) 142-151
50. Clark R.E., Zola S.M., and Squire L.R. Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20 (2000) 8853-8860
51. Broadbent N.J., Squire L.R., and Clark R.E. Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA 101 (2004) 14515-14520
52. Gould T.J., Rowe W.B., Heman K.L., et al. Effects of hippocampal lesions on patterned motor learning in the rat. Brain Res Bull 58 (2002) 581-586
53. Cassaday H.J., and Rawlins J.N. The hippocampus, objects, and their contexts. Behav Neurosci 111 (1997) 1228-1244
54. Aggleton J.P., and Brown M.W. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22 (1999) 425-444 discussion 444-489
55. Mumby D.G., Gaskin S., Glenn M.J., Schramek T.E., and Lehmann H. Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 9 2 (2002) 49-57
56. Ennaceur A., and Delacour J. A new one-trial test for neurobiological studies of memory in rats: 1. Behavioral data. Behav Brain Res 31 (1988) 47-59
57. Jakubowska-Dogru E., Gumusbas U., and Kara F. Individual variation in the spatial reference and working memory assessed under allothetic and idiothetic orientation cues in rat. Acta Neurobiol Exp (Wars) 63 (2003) 17-23
58. Futter J.E., and Aggleton J.P. How rats perform spatial working memory tasks: limitations in the use of egocentric and idiothetic working memory. Q J Exp Psychol (Colchester) 59 (2006) 77-99
59. Barbarosie M., and Avoli M. CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures. J Neurosci 17 (1997) 9308-9314
60. Lebovitz R.M. Autorhythmicity of spontaneous interictal spike discharge at hippocampal penicillin foci. Brain Res 172 (1979) 35-55
61. Prince D.A. Inhibition in "epileptic" neurons. Exp Neurol 21 (1968) 307-321
62. Hablitz J.J. Picrotoxin-induced epileptiform activity in hippocampus: role of endogenous versus synaptic factors. J Neurophysiol 51 (1984) 1011-1027
63. Buzsaki G., Hsu M., Slamka C., Gage F.H., and Horvath Z. Emergence and propagation of interictal spikes in the subcortically denervated hippocampus. Hippocampus 1 (1991) 163-180
64. Shewmon D.A., and Erwin R.J. The effect of focal interictal spikes on perception and reaction time: I. General considerations. Electroencephalogr Clin Neurophysiol 69 (1988) 319-337
65. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99 (1992) 195-231
66. Brashers-Krug T., Shadmehr R., and Bizzi E. Consolidation in human motor memory. Nature 382 (1996) 252-255
67. Walker M.P., Brakefield T., Hobson J.A., and Stickgold R. Dissociable stages of human memory consolidation and reconsolidation. Nature 425 (2003) 616-620
68. Fenn K.M., Nusbaum H.C., and Margoliash D. Consolidation during sleep of perceptual learning of spoken language. Nature 425 (2003) 614-616
69. Gais S., Plihal W., Wagner U., and Born J. Early sleep triggers memory for early visual discrimination skills. Nat Neurosci 3 (2000) 1335-1339
70. Karni A., Tanne D., Rubenstein B.S., Askenasy J.J., and Sagi D. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265 (1994) 679-682
71. Stickgold R., Whidbee D., Schirmer B., Patel V., and Hobson J.A. Visual discrimination task improvement: a multi-step process occurring during sleep. J Cogn Neurosci 12 (2000) 246-254
72. Walker M.P., Brakefield T., Seidman J., Morgan A., Hobson J.A., and Stickgold R. Sleep and the time course of motor skill learning. Learn Mem 10 (2003) 275-284
73. Buzsaki G. Memory consolidation during sleep: a neurophysiological perspective. J Sleep Res 7 Suppl. 1 (1998) 17-23
74. Maquet P. The role of sleep in learning and memory. Science 294 (2001) 1048-1052
75. Buzsaki G. The hippocampo-neocortical dialogue. Cereb Cortex 6 (1996) 81-92
76. Chrobak J.J., Lorincz A., and Buzsaki G. Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus 10 (2000) 457-465
77. Louie K., and Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29 (2001) 145-156
78. Bi G., and Poo M. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24 (2001) 139-166
79. Lorincz A., and Buzsaki G. Two-phase computational model training long-term memories in the entorhinal-hippocampal region. Ann NY Acad Sci 911 (2000) 83-111
80. Shen B., and McNaughton B.L. Modeling the spontaneous reactivation of experience-specific hippocampal cell assembles during sleep. Hippocampus 6 (1996) 685-692
81. Wilson M.A., and McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 265 (1994) 676-679
82. Kali S., and Dayan P. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat Neurosci 7 (2004) 286-294
83. Ribeiro S., Gervasoni D., Soares E.S., et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol 2 1 (2004) E24