Functional network changes in hippocampal CA1 after status epilepticus predict spatial memory deficits in rats

Journal of Neuroscience

Volumn 32, Issue 33, 2012, Pages 11365-11376

  Tyler, Anna L ^a   Matthew Mahoney, J ^a   Richard, Gregory R ^b   Holmes, Gregory L ^a   Lenck Santini, Pierre Pascal ^a   Scott, Rod C ^a,c  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CELL INTERACTION; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DENTATE GYRUS; EPILEPTIC STATE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HISTOLOGY; MALE; NERVE CELL NETWORK; NONBIOLOGICAL MODEL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SINGLE UNIT ACTIVITY; SPATIAL MEMORY; TASK PERFORMANCE;

ANIMALS; CA1 REGION, HIPPOCAMPAL; DISEASE MODELS, ANIMAL; ELECTRODES, IMPLANTED; ENTROPY; IMAGE PROCESSING, COMPUTER-ASSISTED; LITHIUM; MALE; MAZE LEARNING; MEMORY DISORDERS; MODELS, NEUROLOGICAL; MUSCARINIC AGONISTS; NERVE NET; NEURONS; PILOCARPINE; PREDICTIVE VALUE OF TESTS; PROBABILITY; RATS; RATS, SPRAGUE-DAWLEY; SPACE PERCEPTION; STATISTICS AS TOPIC; STATISTICS, NONPARAMETRIC; STATUS EPILEPTICUS;

EID: 84865030854     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1516-12.2012     Document Type: Article

References (42)

1. Bailet LL, Turk WR (2000) The impact of childhood epilepsy on neurocognitive and behavioral performance: a prospective longitudinal study. Epilepsia 41:426-431.
2. Ben-Ari Y (2001) Cell death and synaptic reorganizations produced by seizures. Epilepsia 42 [Suppl 3]:5-7.
3. Bourgeois BF, Prensky AL, Palkes HS, Talent BK, Busch SG (1983) Intelligence in epilepsy: a prospective study in children. Ann Neurol 14: 438-444.
4. Cavalheiro EA, Leite JP, Bortolotto ZA, Turski WA, 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.
5. Cavazos JE, Cross DJ (2006) The role of synaptic reorganization in mesial temporal lobe epilepsy. Epilepsy Behav 8:483-493.
6. Darroch J, Ratcliff D (1972) Generalized iterative scaling for log-linear models. Ann Math Stat 43:1470-1480.
7. DeLorenzo RJ, Hauser WA, Towne AR, Boggs JG, Pellock JM, Penberthy L, Garnett L, Fortner CA, Ko D (1996) A prospective, population-based epidemiologic study of status epilepticus in Richmond, Virginia. Neurology 46:1029-1035.
8. Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1-10.
9. Erdös P, Gallai T (1960) Gráfok elümloírt fokszámú pontokkal. Matematikai Lapok 11:264-274.
10. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680-683.
11. Guzowski JF, McNaughton BL, Barnes CA, Worley PF (1999) Environmentspecific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2:1120-1124.
12. Harris KD, Csicsvari J, Hirase H, Dragoi G, Buzsáki G (2003) Organization of cell assemblies in the hippocampus. Nature 424:552-556.
13. Jambaqué I, Dellatolas G, Dulac O, Ponsot G, Signoret JL (1993) Verbal and visual memory impairment in children with epilepsy. Neuropsychologia 31:1321-1337.
14. Jaynes ET (1957) Information theory and statistical mechanics. Phys Rev 106:620-630.
15. Landau LD, Lifshitz EM (1980) Statistical physics. Oxford, UK: Pergamon.
16. Leite JP, Bortolotto ZA, Cavalheiro EA (1990) Spontaneous recurrent seizures in rats: an experimental model of partial epilepsy. Neurosci Biobehav Rev 14:511-517.
17. Lenck-Santini PP, Holmes GL (2008) Altered phase precession and compression of temporal sequences by place cells in epileptic rats. J Neurosci 28:5053-5062.
18. Lothman EW, Rempe DA, Mangan PS (1995) Changes in excitatory neurotransmission in the CA1 region and dentate gyrus in a chronic model of temporal lobe epilepsy. J Neurophysiol 74:841-848.
19. Mangan PS, Lothman EW (1996) Profound disturbances of preand postsynaptic GABAB- receptor-mediated processes in region CA1 in a chronic model of temporal lobe epilepsy. J Neurophysiol 76:1282-1296.
20. Mangan PS, Rempe DA, Lothman EW (1995) Changes in inhibitory neurotransmission in the ca1 region and dentate gyrus in a chronic model of temporal lobe epilepsy. J Neurophysiol 74:829-840.
21. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34:985-995.
22. Morin F, Beaulieu C, Lacaille JC (1999) Alterations of perisomatic GABA synapses on hippocampal CA1 inhibitory interneurons and pyramidal cells in the kainate model of epilepsy. Neuroscience 93:457-467.
23. Müller CJ, Bankstahl M, Gröticke I, Löscher W (2009) Pilocarpine vs. lithium-pilocarpine for induction of status epilepticus in mice: development of spontaneous seizures, behavioral alterations and neuronal damage. Eur J Pharmacol 619:15-24.
24. Nemenman I (2011) Coincidences and estimation of entropies of random variables with large cardinalities. Entropy 13:2013-2023.
25. Nemenman I, Shafee F, Bialek W (2002) Entropy and inference, revisited. In: Advances in neural information processing systems, Vol. 14 (Dietterich TG, Becker S, Ghahramani Z, ed). Cambridge, MA: MIT.
26. Nemenman I, Bialek W, de Ruyter van Steveninck R (2004) Entropy and information in neural spike trains: progress on the sampling problem. Phys Rev E Stat Nonlin Soft Matter Phys 69:056111.
27. O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
28. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
29. Parent JM (2008) Persistent hippocampal neurogenesis and epilepsy. Epilepsia 49 [Suppl 5]:1-2.
30. Parent JM, Elliott RC, Pleasure SJ, Barbaro NM, Lowenstein DH (2006) Aberrant seizure-induced neurogenesis in experimental temporal lobe epilepsy. Ann Neurol 59:81-91.
31. Schneidman E, Berry MJ 2nd, Segev R, Bialek W (2006) Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440:1007-1012.
32. Scott RC, Gadian DG, King MD, Chong WK, Cox TC, Neville BG, Connelly A (2002) Magnetic resonance imaging findings within 5 days of status epilepticus in childhood. Brain 125:1951-1959.
33. Scott RC, Cross JH, Gadian DG, Jackson GD, Neville BG, Connelly A (2003) Abnormalities in hippocampi remote from the seizure focus: a T2 relaxometry study. Brain 126:1968-1974.
34. Shatskikh T, Zhao Q, Zhou JL, Holmes GL (2009) Effect of topiramate on cognitive function and single units from hippocampal place cells following status epilepticus. Epilepsy Behav 14:40-47.
35. Shlens J, Field GD, Gauthier JL, Grivich MI, Petrusca D, Sher A, Litke AM, Chichilnisky EJ (2006) The structure of multi-neuron firing patterns in primate retina. J Neurosci 26:8254-8266.
36. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.
37. Sutula TP (1991) Reactive changes in epilepsy: cell death and axon sprouting induced by kindling. Epilepsy Res 10:62-70.
38. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L (1989) Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 26:321-330.
39. Tang A, Jackson D, Hobbs J, Chen W, Smith JL, Patel H, Prieto A, Petrusca D, Grivich MI, Sher A, Hottowy P, Dabrowski W, Litke AM, Beggs JM (2008) A maximum entropy model applied to spatial and temporal correlations from cortical networks. in vitro. J Neurosci 28:505-518.
40. Turski WA, Czuczwar SJ, Kleinrok Z, Turski L (1983) Cholinomimetics produce seizures and brain damage in rats. Experientia 39:1408-1411.
41. VanLandingham KE, Heinz ER, Cavazos JE, Lewis DV (1998) Magnetic resonance imaging evidence of hippocampal injury after prolonged focal febrile convulsions. Ann Neurol 43:413-426.
42. Ventura V, Gerkin RC (2012) Accurately estimating neuronal correlation requires a new spikesorting paradigm. Proc Natl Acad Sci U S A 109: 7230-7235.