Electroresponsiveness of medial entorhinal cortex layer III neurons in vitro

Neuroscience

Volumn 81, Issue 4, 1997, Pages 937-950

  Dickson, C T ^a   Mena, A R ^a   Alonso, A ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Brain slice; Epilepsy; Intracellular; Perforant path; Pyramidal cells; Rat

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; DEPOLARIZATION; ENTORHINAL CORTEX; EPILEPSY; HIPPOCAMPUS; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ANIMALS; CALCIUM CHANNELS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; HISTOCYTOCHEMISTRY; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; SODIUM CHANNELS; TETRODOTOXIN;

EID: 0031563760     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00263-7     Document Type: Article

References (88)

1. Alonso A., García-Austt E. Neuronal sources of theta rhythm in the entorhinal cortex of the rat. II. Phase relations between unit discharges and theta field potentials. Expl Brain Res. 67:1987;502-509.
2. Alonso A., Klink R. Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J. Neurophysiol. 70:1993;128-143.
3. Alonso A., Llinás R. Electrophysiology of the mammillary complex in vitro. II. Medial mammillary neurons. J. Neurophysiol. 64:1992;1321-1331.
4. +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature. 342:1989;175-177.
5. Alvarez P., Zola-Morgan S., Squire L. R. Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J. Neurosci. 15:1995;3796-3807.
6. Amaral D. G., Witter M. P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience. 31:1989;571-591.
7. 2-adrenoceptors. J. Neurosci. 4:1984;161-170.
8. Arnold E. S., Hyman B. T., Van Hoesen G. W., Damasio A. Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Archs gen. Psychiat. 48:1991;625-632.
9. Bobinski M., Weigel J., Wisneiski H. M., Tarnawski M., Reisberg B., Mlodzik B., de Leon M. J., Miller D. C. Atrophy of hippocampal formation subdivisions correlates with stage and duration of Alzheimer disease. Dementia. 6:1995;205-210.
10. Bourque C. W., Randle J. C. R., Renaud L. P. Calcium-dependent potassium conductance in rat supraoptic nucleus neurosecretory neurons. J. Neurophysiol. 54:1985;1375-1382.
11. Braak H., Braak E. Entorhinal-hippocampal interaction in mnestic disorders. Hippocampus. 3:1993;239-246.
12. Brankack J., Stewart M., Fox S. E. Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res. 615:1993;310-327.
13. Buhl E. H., Han Z.-S., Lorinczi Z., Stezhka V. V., Karnup S. V., Somogyi P. Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J. Neurophysiol. 71:1994;1289-1307.
14. Buzsáki G., Czopf J., Kondakor I., Kellenyi L. Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current-source density analysis, effects of urethane and atropine. Brain Res. 365:1986;125-137.
15. Buzsáki G., Penttonen M., Gragin A., Nadasdy Z., Chrobak J. Possible physiological role of the perforant path-CA1 projection. Hippocampus. 5:1995;141-146.
16. +-current. J. Neurophysiol. 74:1995;934-941.
17. Charpak S., Pare D., Llinas R. The entorhinal cortex entrains fast CA1 hippocampal oscillations in the anaesthetized guinea-pig: role of the monosynaptic component of the perforant path. Eur. J. Neurosci. 7:1995;1548-1557.
18. Colbert C. M., Levy W. B. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophysiol. 68:1992;1-8.
19. Connors B. W., Gutnick M. J., Prince D. Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48:1982;1302-1320.
20. Connors B. W., Prince D. A. Effects of local anesthetic QX-314 on the membrane properties of hippocampal pyramidal neurons. J. Pharmac. exp. Ther. 220:1982;476-481.
21. Constanti A., Sim J. A. Calcium-dependent potassium conductance in guinea-pig olfactory cortex neurones in vitro. J. Physiol., Lond. 387:1987;173-194.
22. Crill W. E. Persistent sodium current in mammalian central neurons. A. Rev. Physiol. 58:1996;349-362.
23. Dasheiff R. M., McNamara J. O. Electrolytic entorhinal lesions cause seizures. Brain Res. 231:1982;444-450.
24. Deutch C., Spencer S., Robbins R., Cicchetti D., Spencer D. Interictal spikes and hippocampal somatostatin levels in temporal lobe epilepsy. Epilepsia. 32:1991;174-178.
25. Dickson C. T., Alonso A. (1997) Muscarinic induction of synchronous population activity in the entorhinal cortex. J. Neurosci. (in press).
26. Dickson C. T., Kirk I. J., Oddie S. D., Bland B. H. Classification of theta-related cells in the entorhinal cortex: Cell discharges are controlled by the ascending brainstem synchronizing pathway in parallel with hippocampal theta-related cells. Hippocampus. 5:1995;306-319.
27. Doller H. J., Weight F. F. Perforant pathway activation of hippocampal CA1 stratum pyramidal neurons: electrophysiological evidence for a direct pathway. Brain Res. 237:1982;1-13.
28. Du F., Tore E., Kohler C., Lothman E. W., Schwarcz R. Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J. Neurosci. 15:1995;8301-8313.
29. Du F., Whetsell W. O., Abou-Khalil B., Blumenkopf B., Lothman E. W., Schwarcz R. Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy. Epilepsy Res. 16:1993;223-233.
30. Eid T., Du F., Witter M. P. Differential neuronal vulnerability to aminooxyacetic acid and quinolenic acid in the rat parahippocampal region. Neuroscience. 68:1995;645-656.
31. Eid T., Jorritsma-Byham B., Schwarcz R., Witter M. P. Afferents to the seizure-sensitive neurons in layer III of the medial entorhinal area: a tracing study in the rat. Expl Brain Res. 109:1996;209-218.
32. Empson R. M., Heinemann U. The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J. Physiol. 484:1995;707-720.
33. French C. R., Sah P., Buckett K. J., Gage P. W. A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J. gen. Physiol. 95:1990;1139-1157.
34. Glovelli T., Schmitz D., Empson R. M., Dugladze T., Heinemann U. Morphological and electrophysiological characterization of layer III cells of the medial entorhinal cortex of the rat. Neuroscience. 77:1997;629-648.
35. Goldring S., Edwards I., Harding G. W., Bernardo K. L. Results of anterior temporal lobectomy that spares the amygdala in patients with complex partial seizures. J. Neurosurg. 77:1992;185-193.
36. Gomez-Isla T., Price J. L., McKeel D. W. Jr., Morris J. C., Growdon J. H., Hyman B. T. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J. Neurosci. 16:1996;4491-4500.
37. Hotson J. R., Prince D. A. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J. Neurophysiol. 43:1980;409-419.
38. Hyman B. T., Van Hoesen G. W., Damasio A. R. Memory-related neural system in Alzheimer's disease: An anatomic study. Neurology. 40:1990;1721-1730.
39. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. 349:1984;205-226.
40. Jahnsen H., Llinás R. Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J. Physiol. 349:1984;227-247.
41. Jakob H., Beckmann H. Prenatal developmental disturbances in the limbic allocortex in schizophrenics. J. neural. Transm. 65:1986;303-326.
42. Jones R. S. G. Synaptic and intrinsic properties of neurons of origin of the perforant path in layer II of the rat entorhinal cortex in vitro. Hippocampus. 4:1994;335-353.
43. Jones R. S. G., Heinemann U. F. H. and Lambert J. D. C. (1992) The entorhinal cortex and generation of seizure activity: Studies of normal synaptic transmission and epileptogenesis. In Neurotransmitters in Epilepsy (Epilepsy Res. Suppl. 8) (ed. Avanzini G., Engel J. J., Fariello R. and Heinemann U.), pp. 173-180. Elsevier, Amsterdam.
44. Kiss J., Buzsaki G., Morrow J. S., Glantz S. B., Leranth C. Entorhinal cortical innervation of parvalbumin-containing neurons (basket and chandelier cells) in the rat Ammon's horn. Hippocampus. 6:1996;239-246.
45. Klingberg T., Roland P. E., Kawashima R. The human entorhinal cortex participates in associative memory. NeuroReport. 6:1994;57-60.
46. Klink R., Alonso A. Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J. Neurophysiol. 70:1993;144-157.
47. Kunkel D. D., Lacaille J.-C., Schwartzkroin P. A. Ultrastructure of stratum lacunosum-moleculare interneurons of hippocampal CA1 region. Synapse. 2:1988;382-394.
48. Lanthorn T., Storm J., Andersen P. Current-to-frequency transduction in CA1 hippocampal pyramidal cells: slow prepotentials dominate the primary range firing. Expl Brain Res. 53:1984;431-443.
49. Llinas R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. 305:1980;197-213.
50. Llinas R., Sugimori M., Lin J.-W., Cherksey B. Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc. natn. Acad. Sci. U.S.A. 86:1989;1689-1693.
51. Llinas R. R. The intrinsic electrophysiological properties of mammalian neurons: Insights into central nervous system function. Science. 242:1988;1654-1664.
52. Llinás R. R., Alonso A. Electrophysiology of the mammillary complex in vitro. I. Tuberomammillary and lateral mammillary neurons. J. Neurophysiol. 68:1992;1307-1320.
53. Lopes da Silva F. H., Witter M. P., Boeijinga P. H., Lohman H. M. Anatomic organization and physiology of the limbic cortex. Physiol. Rev. 76:1990;453-511.
54. Lorenzon N. M., Foehring R. C. Relationship between repetitive firing and afterhyperpolarizations in human neocortical neurons. J. Neurophysiol. 67:1992;350-363.
55. Mason A., Larkman A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J. Neurosci. 10:1990;1415-1428.
56. McCormick D. A., Connors B. W., Lighthall J. W., Prince D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54:1985;782-806.
57. Mena A., Alonso A. Entorhinal cortex layer III neurons: Characterization and cholinergic excitation. Soc. Neurosci. Abstr. 20:1994;1527.
58. Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 316:1985;440-443.
59. O'Keefe J. and Nadel L. (1978) The Hippocampus as a Cognitive Map. Oxford University Press, Oxford.
60. Paré D., de Curtis M., Llinás R. Role of the hippocampal-entorhinal loop in temporal lobe epilepsy: extra- and intracellular study in the isolated guinea-pig brain in vitro. J. Neurosci. 12:1992;1867-1881.
61. Ramon y Cajal S. (1911) Histologie du Système Nerveux de l'Homme et des Vertébrés. trans. by L. Azoulay. Paris: Maloine 2 vols.
62. Rutecki P. A., Grossman R. G., Armstrong D., Irish-Loewen S. Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. J. Neurosurg. 70:1989;667-675.
63. Ruth R. E., Collier T. J., Routtemberg A. Topography between the entorhinal cortex and the dentate septotemporal axis in rats. I. Medial and intermediate entorhinal projecting cells. J. comp. Neurol. 209:1982;69-78.
64. Ruth R. E., Collier T. J., Routtemberg A. Topographical relationship between the entorhinal cortex and the septotemporal axis of the dentate gyrus in rats. II. Cells projecting from lateral entorhinal subdivisions. J. comp. Neurol. 270:1988;506-516.
65. Scharfman H. E. (1996) Hyperexcitability of entorhinal cortex and hippocampus after application of aminooxyacetic acid (AOAA) to layer III of the rat entorhinal cortex in vitro. J. Neurophysiol. (In press).
66. Schwindt P. C., Spain W. J., Foehring R. C., Stafstrom C. E., Chubb M. C., Crill W. E. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 59:1988;424-449.
67. Scoville W. B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiat. 20:1957;11-21.
68. Soltesz I., Deschênes M. Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J. Neurophysiol. 70:1993;97-116.
69. Spain W. J., Schwindt P. C., Crill W. E. Two transient potassium currents in layer V pyramidal neurones from cat sensorimotor cortex. J. Physiol., Lond. 434:1991;591-607.
70. Spencer S. S., Spencer D. D. Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia. 35:1994;721-727.
71. Squire L. R., Zola-Morgan S. The medial temporal lobe memory system. Science. 253:1991;1380-1386.
72. Stafstrom C. E., Schwindt P., Crill W. E. Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro. Brain Res. 236:1982;221-226.
73. Stafstrom C. E., Schwindt P. C., Chubb M. C., Crill W. E. Properties of persistant sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 53:1985;153-170.
74. Stafstrom C. E., Schwindt P. C., Crill W. E. Repetitive firing in layer V neurons from cat neocortex in vitro. J. Neurophysiol. 52:1984;264-277.
75. Stafstrom C. E., Schwindt P. C., Flatman J. A., Crill W. E. Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 52:1984;244-263.
76. Steward O. Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. comp. Neurol. 167:1976;285-314.
77. Steward O., Scoville S. A. The cells of origin of entorhinal afferents to the hippocampus and fascia dentata of the rat. J. comp. Neurol. 169:1976;347-370.
78. Storm J. F. Action potential repolarization and a fast-hyperpolarization in rat hippocampal pyramidal cells. J. Physiol. 385:1987;733-759.
79. Storm J. F. An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J. Physiol., Lond. 409:1989;171-190.
80. Stringer J. L., Lothman E. W. Reverberatory seizure discharges in hippocampal-parahippocampal circuits. Expl Neurol. 116:1992;198-203.
81. Van Hoesen G. W., Hyman B. T., Damasio A. R. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus. 1:1991;1-8.
82. Walther H., Lambert J.D.C., Jones R.S.G., Heinemann U., Hamon B. Epileptiform activity in combined slices of the hippocampus, subiculum and entorhinal cortex during perfusion with low magnesium medium. Neurosci. Lett. 69:1986;156-161.
83. Wilson W. A., Swartzwelder H. S., Anderson W. W., Lewis D. V. Seizure activity in vitro: A dual focus model. Epilepsy Res. 2:1988;289-293.
84. Witter M. P., Griffioen A. W., Jorritsma-Byham B., Krijnen J. L. M. Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci. Lett. 85:1988;193-198.
85. Witter M. P., Groenewegen H. J., Lopes da Silva F. H., Lohman A. H. M. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33:1989;161-253.
86. Yarom Y., Sugimori M., Llinas R. Ionic currents and firing patterns of mammalian vagal motoneurons in vitro. Neuroscience. 16:1985;719-737.
87. Yeckel M. F., Berger T. W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc. natn. Acad. Sci. U.S.A. 87:1990;5832-5836.
88. Zola-Morgan S., Squire L. R. Neuroanatomy of memory. A. Rev. Neurosci. 16:1993;547-563.