Diversity and excitability of deep-layer entorhinal cortical neurons in a model of temporal lobe epilepsy

Journal of Neurophysiology

Volumn 108, Issue 6, 2012, Pages 1724-1738

  Pilli, Jyotsna ^a   Abbasi, Saad ^a   Richardson, Max ^a   Kumar, Sanjay S ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Cell type classification; Entorhinal cortex; Excitatory neurons

Indexed keywords

PILOCARPINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; MALE; NERVE CELL; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; STELLATE CELL; SYNAPSE; TEMPORAL LOBE EPILEPSY;

ACTION POTENTIALS; ANIMALS; DENDRITES; DISEASE MODELS, ANIMAL; ENTORHINAL CORTEX; EPILEPSY, TEMPORAL LOBE; GABAERGIC NEURONS; HIPPOCAMPUS; INTERNEURONS; MALE; PILOCARPINE; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 84866391535     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00364.2012     Document Type: Article

References (81)

1. Agmon A, Connors BW. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci 12: 319-329, 1992.
2. Agmon A, Connors BW. Repetitive burst-firing neurons in the deep layers of mouse somatosensory cortex. Neurosci Lett 99: 137-141, 1989.
3. Agrawal N, Alonso A, Ragsdale DS. Increased persistent sodium currents in rat entorhinal cortex layer V neurons in a post-status epilepticus model of temporal lobe epilepsy. Epilepsia 44: 1601-1604, 2003.
4. Alonso A, Klink R. Differential electroresponsiveness of stellate and pyramidal- like cells of medial entorhinal cortex layer II. J Neurophysiol 70: 128-143, 1993.
5. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides- Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvarday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Munoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9: 557-568, 2008.
6. Bartesaghi R, Gessi T, Sperti L. Electrophysiological analysis of the hippocampal projections to the entorhinal area. Neuroscience 30: 51-62, 1989.
7. Bartolomei F, Khalil M, Wendling F, Sontheimer A, Regis J, Ranjeva JP, Guye M, Chauvel P. Entorhinal cortex involvement in human mesial temporal lobe epilepsy: an electrophysiologic and volumetric study. Epilepsia 46: 677-687, 2005.
8. Bean BP. The action potential in mammalian central neurons. Nat Rev Neurosci 8: 451-465, 2007.
9. Bear J, Fountain NB, Lothman EW. Responses of the superficial entorhinal cortex in vitro in slices from naive and chronically epileptic rats. J Neurophysiol 76: 2928-2940, 1996.
10. Bragin A, Jando G, Nadasdy Z, van Landeghem M, Buzsaki G. Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J Neurophysiol 73: 1691-1705, 1995.
11. Bragin DE, Sanderson JL, Peterson S, Connor JA, Muller WS. Development of epileptiform excitability in the deep entorhinal cortex after status epilepticus. Eur J Neurosci 30: 611-624, 2009.
12. + conductances with complementary functions in postsynaptic integration at a central auditory synapse. J Neurosci 15: 8011-8022, 1995.
13. Buckmaster PS, Alonso A, Canfield DR, Amaral DG. Dendritic morphology, local circuitry, and intrinsic electrophysiology of principal neurons in the entorhinal cortex of macaque monkeys. J Comp Neurol 470: 317-329, 2004.
14. Buckmaster PS, Dudek FE. Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization. J Neurophysiol 77: 2685-2696, 1997.
15. Burns R. Cluster analysis. In: Business Research Methods and Statistics Using SPSS. London: SAGE, 2008, p. 552-558.
16. Burwell RD, Amaral DG. Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J Comp Neurol 391: 293-321, 1998.
17. Buzsaki G. The hippocampo-neocortical dialogue. Cereb Cortex 6: 81-92, 1996.
18. Canto CB, Witter MP. Cellular properties of principal neurons in the rat entorhinal cortex. II. The medial entorhinal cortex. Hippocampus 22: 1277-1299, 2012.
19. Cauli B, Porter JT, Tsuzuki K, Lambolez B, Rossier J, Quenet B, Audinat E. Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci USA 97: 6144-6149, 2000.
20. Chrobak JJ, Buzsaki G. Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14: 6160-6170, 1994.
21. Chrobak JJ, Lorincz A, Buzsaki G. Physiological patterns in the hippocampo- entorhinal cortex system. Hippocampus 10: 457-465, 2000.
22. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99-104, 1990.
23. Connors BW, Gutnick MJ, Prince DA. Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48: 1302-1320, 1982.
24. de Guzman P, Inaba Y, Baldelli E, de Curtis M, Biagini G, Avoli M. Network hyperexcitability within the deep layers of the pilocarpine-treated rat entorhinal cortex. J Physiol 586: 1867-1883, 2008.
25. Deadwyler SA, West JR, Cotman CW, Lynch G. Physiological studies of the reciprocal connections between the hippocampus and entorhinal cortex. Exp Neurol 49: 35-57, 1975.
26. Deller T, Martinez A, Nitsch R, Frotscher M. A novel entorhinal projection to the rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic neurons. J Neurosci 16: 3322-3333, 1996.
27. Dhillon A, Jones RS. Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99: 413-422, 2000.
28. Dickson CT, Alonso A. Muscarinic induction of synchronous population activity in the entorhinal cortex. J Neurosci 17: 6729-6744, 1997.
29. Dickson CT, Magistretti J, Shalinsky M, Hamam B, Alonso A. Oscillatory activity in entorhinal neurons and circuits. Mechanisms and function. Ann NY Acad Sci 911: 127-150, 2000.
30. Dickson CT, Mena AR, Alonso A. Electroresponsiveness of medial entorhinal cortex layer III neurons in vitro. Neuroscience 81: 937-950, 1997.
31. Dolorfo CL, Amaral DG. Entorhinal cortex of the rat: organization of intrinsic connections. J Comp Neurol 398: 49-82, 1998.
32. Du F, Eid T, Lothman EW, Kohler C, Schwarcz R. Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J Neurosci 15: 6301-6313, 1995.
33. Du F, Whetsell WO Jr, Abou-Khalil B, Blumenkopf B, Lothman EW, Schwarcz R. Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy. Epilepsy Res 16: 223-233, 1993.
34. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA. Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178, 2002.
35. Engel J, Pedley TA, Aicardi J. Epilepsy: a Comprehensive Textbook. Philadelphia, PA: Lippincott-Raven, 1998.
36. Garden DL, Dodson PD, O'Donnell C, White MD, Nolan MF. Tuning of synaptic integration in the medial entorhinal cortex to the organization of grid cell firing fields. Neuron 60: 875-889, 2008.
37. Giocomo LM, Zilli EA, Fransen E, Hasselmo ME. Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315: 1719-1722, 2007.
38. Gloveli T, Dugladze T, Schmitz D, Heinemann U. Properties of entorhinal cortex deep layer neurons projecting to the rat dentate gyrus. Eur J Neurosci 13: 413-420, 2001.
39. 2+]i signalling in projection cells of medial entorhinal cortex layers II and III. Eur J Neurosci 11: 3626-3636, 1999.
40. Gloveli T, Schmitz D, Heinemann U. Prolonged inhibitory potentials in layer III projection cells of the rat medial entorhinal cortex induced by synaptic stimulation in vitro. Neuroscience 80: 119-131, 1997.
41. Gutnick MJ, Connors BW, Prince DA. Mechanisms of neocortical epileptogenesis in vitro. J Neurophysiol 48: 1321-1335, 1982.
42. Halabisky B, Shen F, Huguenard JR, Prince DA. Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol 96: 834-845, 2006.
43. Hamam BN, Kennedy TE, Alonso A, Amaral DG. Morphological and electrophysiological characteristics of layer V neurons of the rat medial entorhinal cortex. J Comp Neurol 418: 457-472, 2000.
44. Hargus NJ, Merrick EC, Nigam A, Kalmar CL, Baheti AR, Bertram EH 3rd, Patel MK. Temporal lobe epilepsy induces intrinsic alterations in Na channel gating in layer II medial entorhinal cortex neurons. Neurobiol Dis 41: 361-376, 2010.
45. Iijima T, Witter MP, Ichikawa M, Tominaga T, Kajiwara R, Matsumoto G. Entorhinal-hippocampal interactions revealed by real-time imaging. Science 272: 1176-1179, 1996.
46. Jones RS. Entorhinal-hippocampal connections: a speculative view of their function. Trends Neurosci 16: 58-64, 1993.
47. Jones RS, Heinemann U. Synaptic and intrinsic responses of medical entorhinal cortical cells in normal and magnesium-free medium in vitro. J Neurophysiol 59: 1476-1496, 1988.
48. Jones RS, Lambert JD. The role of excitatory amino acid receptors in the propagation of epileptiform discharges from the entorhinal cortex to the dentate gyrus in vitro. Exp Brain Res 80: 310-322, 1990a.
49. Jones RS, Lambert JD. Synchronous discharges in the rat entorhinal cortex in vitro: site of initiation and the role of excitatory amino acid receptors. Neuroscience 34: 657-670, 1990b.
50. Jutila L, Ylinen A, Partanen K, Alafuzoff I, Mervaala E, Partanen J, Vapalahti M, Vainio P, Pitkanen A. MR volumetry of the entorhinal, perirhinal, and temporopolar cortices in drug-refractory temporal lobe epilepsy. Am J Neuroradiol 22: 1490-1501, 2001.
51. Kandel ER, Spencer WA. Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. J Neurophysiol 24: 243-259, 1961.
52. Klink R, Alonso A. Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex. Hippocampus 7: 571-583, 1997.
53. Kloosterman F, Witter MP, Van Haeften T. Topographical and laminar organization of subicular projections to the parahippocampal region of the rat. J Comp Neurol 455: 156-171, 2003.
54. Kohler C. Intrinsic connections of the retrohippocampal region in the rat brain. II. The medial entorhinal area. J Comp Neurol 246: 149-169, 1986.
55. Kohler C. A projection from the deep layers of the entorhinal area to the hippocampal formation in the rat brain. Neurosci Lett 56: 13-19, 1985.
56. Kumar SS, Buckmaster PS. Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 26: 4613-4623, 2006.
57. Kumar SS, Jin X, Buckmaster PS, Huguenard JR. Recurrent circuits in layer II of medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 27: 1239-1246, 2007.
58. Le Bon-Jego M, Yuste R. Persistently active, pacemaker-like neurons in neocortex. Front Neurosci 1: 123-129, 2007.
59. Lingenhohl K, Finch DM. Morphological characterization of rat entorhinal neurons in vivo: soma-dendritic structure and axonal domains. Exp Brain Res 84: 57-74, 1991.
60. Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AH. Anatomic organization and physiology of the limbic cortex. Physiol Rev 70: 453-511, 1990.
61. Menendez de la Prida L, Suarez F, Pozo MA. Electrophysiological and morphological diversity of neurons from the rat subicular complex in vitro. Hippocampus 13: 728-744, 2003.
62. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294, 1972.
63. Ribak CE, Seress L, Weber P, Epstein CM, Henry TR, Bakay RA. Alumina gel injections into the temporal lobe of rhesus monkeys cause complex partial seizures and morphological changes found in human temporal lobe epilepsy. J Comp Neurol 401: 266-290, 1998.
64. Rutecki PA, Grossman RG, Armstrong D, Irish-Loewen S. Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. J Neurosurg 70: 667-675, 1989.
65. Scharfman HE, Goodman JH, Du F, Schwarcz R. Chronic changes in synaptic responses of entorhinal and hippocampal neurons after aminooxyacetic acid (AOAA)-induced entorhinal cortical neuron loss. J Neurophysiol 80: 3031-3046, 1998.
66. Sloviter RS. Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1: 41-66, 1991.
67. Smith BN, Dudek FE. Short- and long-term changes in CA1 network excitability after kainate treatment in rats. J Neurophysiol 85: 1-9, 2001.
68. Steriade M. Neocortical cell classes are flexible entities. Nat Rev Neurosci 5: 121-134, 2004.
69. Stewart M. Columnar activity supports propagation of population bursts in slices of rat entorhinal cortex. Brain Res 830: 274-284, 1999.
70. Thorndike RL. Who belongs in the family? Psychometrika 18: 267-276, 1953.
71. Tolner EA, Kloosterman F, van Vliet EA, Witter MP, Silva FH, Gorter JA. Presubiculum stimulation in vivo evokes distinct oscillations in superficial and deep entorhinal cortex layers in chronic epileptic rats. J Neurosci 25: 8755-8765, 2005.
72. Turski L, Ikonomidou C, Turski WA, Bortolotto ZA, Cavalheiro EA. Review: cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy. Synapse 3: 154-171, 1989.
73. van der Linden S, Lopes da Silva FH. Comparison of the electrophysiology and morphology of layers III and II neurons of the rat medial entorhinal cortex in vitro. Eur J Neurosci 10: 1479-1489, 1998.
74. van Haeften T, Baks-te-Bulte L, Goede PH, Wouterlood FG, Witter MP. Morphological and numerical analysis of synaptic interactions between neurons in deep and superficial layers of the entorhinal cortex of the rat. Hippocampus 13: 943-952, 2003.
75. van Haeften T, Jorritsma-Byham B, Witter MP. Quantitative morphological analysis of subicular terminals in the rat entorhinal cortex. Hippocampus 5: 452-459, 1995.
76. Ward JH Jr. Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58: 234-236, 1963.
77. Wilson CL, Isokawa M, Babb TL, Crandall PH. Functional connections in the human temporal lobe. I. Analysis of limbic system pathways using neuronal responses evoked by electrical stimulation. Exp Brain Res 82: 279-292, 1990.
78. Witter MP. Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 3 Spec No: 33-44, 1993.
79. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33: 161-253, 1989.
80. Wouterlood FG. Spotlight on the neurons (1): Cell types, local connectivity, microcircuits, and distribution of markers. In: The Parahippocampal Region: Organization and Role in Cognitive Function, edited by Witter MP, Wouterlood FG. Oxford, UK: Oxford Univ. Press, 2002, p. 61-88.
81. Yang J, Woodhall GL, Jones RS. Tonic facilitation of glutamate release by presynaptic NR2B-containing NMDA receptors is increased in the entorhinal cortex of chronically epileptic rats. J Neurosci 26: 406-410, 2006.