Advertisement

Brain Slices pp 155-199 | Cite as

Hippocampus

Electrophysiological Studies of Epileptiform Activity in Vitro
  • Bradley E. Alger

Abstract

Studies on epileptic phenomena have multiplied rapidly with the growing realization that many of the persistent problems in the field can be attacked directly using the in vitro slice preparation. Recently, the hip-pocampal slice has been most widely used in studies of epilepsy for reasons that are detailed in the Appendix. While attempting to present an overview of electrophysiological studies of epilepsy in the hippo-campal slice, this review will focus on data that has appeared since 1978. The fundamental hypothesis concerning the intrinsic nature of the epileptiform “burst” potential has been widely supported (see Prince, 1978; Schwartzkroin and Wyler, 1980). The chief areas of departure of the present discussion from previous reviews will be in consideration of data pertaining to: (1) the existence of “giant excitatory postsynaptic potentials (EPSPs),” (2) modes of inhibitory synaptic control over pyramidal cell dendrites, (3) the nature of various afterhyperpolarizations, (4) ways in which synchronization of firing within a neuronal population can occur, and (5) mechanisms that can enable epileptic discharges to spread.

Keywords

Pyramidal Cell Hippocampal Slice Epileptiform Activity Hippocampal Pyramidal Cell Interictal Spike 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alger, B. E., 1983, Characteristics of a slow hyperpolarizing synaptic potential in rat hippocampal pyramidal cells, J. Neurophysiol., in press.Google Scholar
  2. Alger, B. E. and Nicoll, R. A., 1979, GABA-mediated biphasic inhibitory responses in hippocampus, Nature (London) 281:315–317.CrossRefGoogle Scholar
  3. Alger, B. E. and Nicoll, R. A., 1980a, The epileptiform burst afterhyperpolarization: A calcium-dependent potassium potential in hippocampal pyramidal cells, Science, 210:1122–1124.PubMedCrossRefGoogle Scholar
  4. Alger, B. E. and Nicoll, R. A., 1980b, Spontaneous inhibitory post-synaptic potentials in hippocampus, Brain Res. 200:195–200.PubMedCrossRefGoogle Scholar
  5. Alger, B. E. and Nicoll, R. A., 1981, Epileptiform burst termination and the AHP in hippocampal CA1 pyramidal cells, Neurosci Abstr. 7:629.Google Scholar
  6. Alger, B. E. and Nicoll, R. A., 1982a, Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied in vitro, J. Physiol. (London) 328:123–141.Google Scholar
  7. Alger, B. E. and Nicoll, R. A., 1982b, Feedforward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro, J. Physiol. (London) 328:105–123.Google Scholar
  8. Alger, B. E. and Nicoll, R. A., 1983, Ammonia does not selectively block IPSPs in rat hippocampal pyramidal cells, J. Neurophysiol. 49:1381–1390.PubMedGoogle Scholar
  9. Alger, B. E., McCarren, M., and Fisher, R. S., 1983, On the possibility of simultaneously recording from two cells with a single microelectrode in the hippocampal slice, Brain Res., 270:137–141.PubMedCrossRefGoogle Scholar
  10. Allen, G. I., Eccles, J. C., Nicoll, R. A., Oshima, T., and Rubia, F. J., 1977, The ionic mechanisms concerned in generating the IPSPs of hippocampal pyramidal cells, Proc. R. Soc. London, set. B 198:363–384.CrossRefGoogle Scholar
  11. Andersen, P., 1976, Some properties of synapses near to and far from the soma of hippocampal pyramids, Exp. Brain Res. 1 (Suppl.):202–206.Google Scholar
  12. Andersen, P., Eccles, J. C., and Loyning, Y., 1964a, Location of postsynaptic inhibitory synapses on hippocampal pyramids, J. Neurophysiol. 27:592–607.PubMedGoogle Scholar
  13. Andersen, P., Eccles, J. C., and Loyning, Y. 1964b, Pathway of postsynaptic inhibition in hippocampal pyramids, J. Neurophysiol. 27:608–619.PubMedGoogle Scholar
  14. Andersen, P., Gross, G. N., Lomo, T., and Sveen, O., 1969, Participation of inhibitory and excitatory interneurones in the control of hippocampal cortical output, in: The Interneuron, UCLA Forum for Medical Science, No. 11 (M. A. B. Brazier, ed.), University of California Press, Los Angeles, pp. 415–467.Google Scholar
  15. Andersen, P., Bliss, T. V. P., and Skrede, K. K., 1971, Unit analysis of hippocampal population spikes, Exp. Brain Res. 13:208–221.PubMedGoogle Scholar
  16. Andersen, P., Gjerstad, L., and Langmoen, I. A., 1978, A cortical epilepsy model in vitro, in: Abnormal Neuronal Discharges (N. Chalazonitis and M. Buisson, eds.), Raven Press, New York, pp. 29–36.Google Scholar
  17. Andersen, P., Dingledine, R., Gjerstad, L., Langmoen, I. A., and Mosfeldt-Laursen, A., 1980, Two different responses of hippocampal pyramidal cells to application of gamma-aminobutyric acid, J. Physiol. (London) 305:279–296.Google Scholar
  18. Andrew, R. D., Taylor, C. P., Snow, R. W., and Dudek, F. E., 1981, Coupling in rat hippocampal slices: Dye transfer between CA1 pyramidal cells, Brain Res. Bull. 8:211–222.CrossRefGoogle Scholar
  19. Ascher, P., Marty, A., and Neild, T. O., 1978, Lifetime and elementary conductance of the channels mediating the excitatory effects of acetylcholine in Aplysia neurones, J. Physiol. (London) 278:177–206.Google Scholar
  20. Ayala, G. F., Dichter, M., Gumnit, R. J., Matsumoto, H., and Spencer, W. A., 1973, Genesis of epileptic interictal spikes: New knowledge of cortical feedback systems suggests a neurophysiological explanation of brief paroxysms, Brain Res. 52:1–17.PubMedCrossRefGoogle Scholar
  21. Benardo, L. S., and Prince, D. A., 1981, Acetylcholine induced modulation of hippocampal pyramidal neurons, Brain Res. 211:227–234.PubMedCrossRefGoogle Scholar
  22. Ben-Ari, Y., Krnjevic, K., and Reinhardt, W., 1979, Hippocampal seizures and failure of inhibition, Can. J. Physiol. Pharmacol. 57:1462–1466.CrossRefGoogle Scholar
  23. Ben-Ari, Y., Krnjevic K., Reinhardt, W., and Ropert, N., 1981, Intracellular observations on the disinhibitory action of acetylcholine in the hippocampus, Neuroscience 6:2475–2484.PubMedCrossRefGoogle Scholar
  24. Benninger, C., Kadis, J., and Prince, D. A., 1980, Extracellular calcium and potassium changes in hippocampal slices, Brain Res. 187:105–182.CrossRefGoogle Scholar
  25. Binstock, L. and Lecar, H., 1969, Ammonium ion currents in the squid giant axon, J. Gen. Physiol. 53:342–361.PubMedCrossRefGoogle Scholar
  26. Brown, D. A. and Adams, P. R., 1980, Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone, Nature (London), 283:673–676.CrossRefGoogle Scholar
  27. Brown, T. H., Wong, R. K. S., and Prince, D. A., 1979, Spontaneous miniature synaptic potentials in hippocampal neurons, Brain Res. 177:194–199.PubMedCrossRefGoogle Scholar
  28. Brown, T. H., Fricke, R. A., and Perkel, D. H., 1981, Passive electrical constants in three classes of hippocampal neurons, J. Neurophysiol. 46:812–827.PubMedGoogle Scholar
  29. Chestnut, R. M. and Schwartzkroin, P. A., 1982, Responses to GABA in developing rabbit hippocampus, Neurosci. Abstr. 8:326.Google Scholar
  30. Constanti, A., Connor, J. D., Galvan, M., and Nistri, A., 1980, Intracellularly-recorded effects of glutamate and aspartate on neurones in the guinea-pig olfactory cortex, Brain Res. 195:403–420.PubMedCrossRefGoogle Scholar
  31. Corrigall, W. A. and Linseman, M. A., 1980, A specific effect of morphine on evoked activity in the rat hippocampal slice, Brain Res. 192:227–238.PubMedCrossRefGoogle Scholar
  32. Dingledine, R. and Gjerstad, L., 1980, Reduced inhibition during epileptiform activity in the in vitro hippocampal slice, J. Physiol. (London) 305:297–313.Google Scholar
  33. Djorup, A., Jahnsen, H., and Mosfeldt-Laursen, A., 1981, The dendritic response to GABA in CA1 of the hippocampal slice, Brain Res. 219:196–201.PubMedCrossRefGoogle Scholar
  34. Dodd, J., Dingledine, R., and Kelly, J. S., 1981, The excitatory action of acetylcholine on hippocampal neurones of the guinea pig and rat maintained in vitro, Brain Res. 207:109–127.PubMedCrossRefGoogle Scholar
  35. Dunwiddie, T., Mueller, A., Palmer, M., Stewart, J., and Hoffer, B., 1980, Electrophysiological interactions of enkephalins with neuronal circuitry in the rat hippocampus. I. Effects on pyramidal cell activity, Brain Res. 184:311–330.PubMedCrossRefGoogle Scholar
  36. Eccles, J. C., 1964, The Physiology of Synapses, Springer-Verlag, New York.CrossRefGoogle Scholar
  37. Erlich, M., Plum, F., and Duffy, T. E., 1980, Blood and brain ammonia concentrations after portacaval anastomosis. Effects of acute ammonia loading, J. Neurochem. 34:1538–1542.CrossRefGoogle Scholar
  38. Fujita, Y., 1975, Two types of depolarizing after-potentials in hippocampal pyramidal cells of rabbits, Brain Res. 94:435–446.PubMedCrossRefGoogle Scholar
  39. Fujita, Y., 1979, Evidence for the existence of inhibitory postsynaptic potentials in dendrites and their functional significance in hippocampal pyramidal cells of adult rabbits, Brain Res. 175:59–69.PubMedCrossRefGoogle Scholar
  40. Fujita, Y. and Iwasa, H., 1977, Electrophysiological properties of so-called inactivation response and their relationship to dendritic activity in hippocampal pyramidal cells of rabbits, Brain Res. 130:89–100.PubMedCrossRefGoogle Scholar
  41. Gjerstad, L., Andersen, P., Langmoen, I. A., Lundervold, A., and Hablitz, J. J., 1981, Synaptic triggering of epileptiform discharges in CA1 pyramidal cells in vitro, Acta Physiol. Scand. 113:245–252.PubMedCrossRefGoogle Scholar
  42. Gustafsson, B. and Wigstrom, H., 1981, Evidence for two types of afterhyperpolarization in CA1 pyramidal cells in the hippocampus, Brain Res. 206:462–468.PubMedCrossRefGoogle Scholar
  43. Gutnick, M. J. and Prince, D. A., 1981, Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice, Science 211:67–70.PubMedCrossRefGoogle Scholar
  44. Haas, H. L., 1982, Cholinergic disinhibition in hippocampal slices of the rat, Brain Res. 233:200–204.PubMedCrossRefGoogle Scholar
  45. Hablitz, J. J., 1981, Effects of intracellular injections of chloride and EGTA on postepileptiform-burst hyperpolarizations in hippocampal neurons, Neurosci. Lett. 22:159–163.PubMedCrossRefGoogle Scholar
  46. Hablitz, J. J. and Andersen, P., 1982, Effect of sodium ions on penicillin-induced epileptiform activity in vitro, Exp. Brain Res. 47:154–157.Google Scholar
  47. Hablitz, J. J. and Langmoen, I. A., 1982, Excitation of hippocampal pyramidal cells byglutamate in the guinea pig and rat, J. Physiol. (London) 325:317–331.Google Scholar
  48. Hablitz, J. J. and Lundervold, A., 1981, Hippocampal excitability and changes in extracellular potassium, Exp. Neurol 71:410–420.PubMedCrossRefGoogle Scholar
  49. Halliwell, J. V. and Adams, P. R., 1982, Voltage clamp analysis of muscarinic excitation in hippocampal neurons, Brain Res. 250:71–92.PubMedCrossRefGoogle Scholar
  50. Hori, N. and Katsuda, N., 1978, Electrophysiological studies on the depolarization shift of hippocampal pyramidal cells in vitro: The nature of the long duration hyperpolar- ization, in: Integrative Functions of the Nervous System, Volume 1 (M. Ito, N. Tsukahara, K. Kubota, and K. Yagi, eds.), Kodansha, Tokyo, pp. 345–347.Google Scholar
  51. Hotson, J. R. and Prince, D. A., 1980, A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons, J. Neurophysiol. 43:409–419.PubMedGoogle Scholar
  52. Hotson, J. R. and Prince, D. A., 1981, Penicillin- and barium-induced epileptiform bursting in hippocampal neurons: Actions on Ca++ and K+ potentials, Ann. Neurol. 10:11–17.PubMedCrossRefGoogle Scholar
  53. Hotson, J. R., Prince, D. A., and Schwartzkroin, P. A., 1979, Anomalous inward rectification in hippocampal neurons, J. Neurophysiol. 42:889–895.PubMedGoogle Scholar
  54. Hounsgaard, J., 1978, Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus, Exp. Neurol. 62:787–797.PubMedCrossRefGoogle Scholar
  55. Iles, J. F. and Jack, J. J. B., 1980, Ammonia: Assessment of its action on postsynaptic inhibition as a cause of convulsions, Brain 103:555–578.PubMedCrossRefGoogle Scholar
  56. Jahnsen, H. and Mosfeldt-Laursen, A., 1981, The effects of a benzodiazepine on the hy-perpolarizing and the depolarizing responses of hippocampal cells to GABA, Brain Res. 207:214–217.PubMedCrossRefGoogle Scholar
  57. Jefferys, J. G. R. and Haas, H. L., 1982, Synchronized bursting of CA1 hippocampal pyramidal sells in the absence of synaptic transmission, Nature 300:448–450.PubMedCrossRefGoogle Scholar
  58. Johnston, D. and Brown, T. H., 1981, Giant synaptic potential hypothesis for epileptiform activity, Science 211:294–297.PubMedCrossRefGoogle Scholar
  59. Johnston, D. J., 1981, Passive cable properties of hippocampal CA3 pyramidal neurons, Cell. Mol Neurobiol. 1:41–55.PubMedCrossRefGoogle Scholar
  60. Johnston, D., Hablitz, J. J., and Wilson, W., 1980, Voltage clamp discloses slow inward current in hippocampal burst-firing neurones, Nature (London) 286:391–393.CrossRefGoogle Scholar
  61. Kandel, E. R. and Spencer, W. A., 1961, Electrophysiology of hippocampal neurons. II. Afterpotentials and repetitive firing, J. Neurophysiol. 24:243–259.PubMedGoogle Scholar
  62. Kandel, E. R., Spencer, W. A., and Brinley, F. J., 1961, Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization, J. Neurophysiol. 24:225–242.PubMedGoogle Scholar
  63. Knowles, W. D. and Schwartzkroin, P. A., 1981, Local circuit synaptic interactions in hippocampal brain slices, J. Neurosci. 1:318–322.PubMedGoogle Scholar
  64. Knowles, W. D., Funch, P. G., and Schwartzkroin, P. A., 1982, Electrotonic and dye coupling in hippocampal CA1 pyramidal cells in vitro, Neuroscience 7:1713–1722.PubMedCrossRefGoogle Scholar
  65. Krnjevic, K. and Ropert, N., 1981, Septo-hippocampal pathway modulates hippocampal activity by a cholinergic mechanism, Can. J. Physiol. Pharmacol. 59:911–914.PubMedCrossRefGoogle Scholar
  66. Krnjevic, K. K., Reiffenstein, R. J., and Ropert, N., 1981, Disinhibitory action of acetylcholine in the rat hippocampus: Extracellular observations, Neuroscience 6:2465–2474.PubMedCrossRefGoogle Scholar
  67. Langmoen, I. A., Andersen, P., Gjerstad, L., Mosfeldt-Laursen, A., and Ganes, T., 1978, Two separate effects of GABA on hippocampal pyramidal cells in vitro, Acta Physiol. Scand. 102:C27.Google Scholar
  68. Lee, H. K., Dunwiddie, T., and Hoffer, B., 1980, Electrophysiological interactions of enkephalins with neuronal circuitry in the rat hippocampus. II. Effects of interneuron excitability, Brain Res. 184:331–342.PubMedCrossRefGoogle Scholar
  69. Leung, L. S., 1978, Hippocampal CA1 region demonstration of antidromic dendritic spike and dendritic inhibition, Brain Res. 158:219–222.PubMedCrossRefGoogle Scholar
  70. Llinás, R., Baker, R., and Precht, W., 1974a, Blockage of inhibition by ammonium acetate action on Cl-pump in cat trochlear motoneurons, J. Neurophysiol. 37:522–533.PubMedGoogle Scholar
  71. Llinás, R., Baker and Sotelo, C., 1974b, Electrotonic coupling between neurons in cat inferior olive, J. Neurophysiol. 38:541–560.Google Scholar
  72. Lockwood, A. H., McDonald, J. M., Reiman, R. E., Gelbard, A. S., Laughlin, J. S., Duffy, T. E., and Plum, F., 1979, The dynamics of ammonia metabolism in man, J. Clin. Invest. 63:449–460.PubMedCrossRefGoogle Scholar
  73. Lorente de Nó, R., 1934, Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system, J. Psychol. Neurol. 46:113–177.Google Scholar
  74. Lux, H. D., 1971, Ammonium and chloride extrusion: Hyperpolarizing synaptic inhibition in spinal motoneurons, Science 173:555–557.PubMedCrossRefGoogle Scholar
  75. Lynch, G. S., Jensen, R. A., McGaugh, J. L., Davila, K., and Oliver, M. W., 1981, Effects of enkephalin, morphine and naloxone on the electrical activity of the in vitro hippocampal slice preparation, Exp. Neurol. 71:527–540.PubMedCrossRefGoogle Scholar
  76. MacVicar, B. A. and Dudek, F. E., 1980a, Local synaptic circuits in rat hippocampus: Interactions between pyramidal cells, Brain Res. 184:220–223.PubMedCrossRefGoogle Scholar
  77. MacVicar, B. A. and Dudek, F. E., 1980b, Dye coupling between CA3 pyramidal cells in slices of rat hippocampus, Brain Res. 196:494–497.PubMedCrossRefGoogle Scholar
  78. MacVicar, B. A. and Dudek, F. E., 1981, Electrotonic coupling between pyramidal cells: A direct demonstration in rat hippocampal slices, Science 213:782–784.PubMedCrossRefGoogle Scholar
  79. Madison, D. V. and Nicoll, R. A., 1982, Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus, Nature (London) 299:636–638.CrossRefGoogle Scholar
  80. Matthews, G. and Wickelgren, W. O., 1979, Glycine, GABA and synaptic inhibition of reticulospinal neurones of lamprey, J. Physiol. 293:393–415.PubMedGoogle Scholar
  81. Mesher, R. A. and Schwartzkroin, P. A., 1980, Can CA3 epileptiform discharge induce bursting in normal CA1 hippocampal neurons? Brain Res. 183:472–476.PubMedCrossRefGoogle Scholar
  82. Newberry, N. R. and Nicoll, R. A., 1982, Properties of the late hyperpolarizing potential in hippocampal pyramidal cells in vitro, Neurosci. Abstr. 8:412.Google Scholar
  83. Nicoll, R. A. and Alger, B. E., 1981, Synaptic excitation may activate a calcium dependent potassium conductance in hippocampal pyramidal cells, Science 212:957–959.PubMedCrossRefGoogle Scholar
  84. Nicoll, R. A., Eccles, J. C., Oshima, T., and Rubia, F., 1975, Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates, Nature (London) 258:625–627.CrossRefGoogle Scholar
  85. Nicoll, R. A., Siggins, G. R., Ling, N., Bloom, F. E., and Guillemin, R., 1977, Neuronal actions of endorphins and enkephalins among brain regions: A comparative microiontophoretic study, Proc. Natl. Acad. Sci. USA 74:2584–2588.PubMedCrossRefGoogle Scholar
  86. Nicoll, R. A., Alger, B. E., and Jahr, C. E., 1980, Enkephalin blocks inhibitory pathways in the vertebrate central neurons system, Nature (London) 287:22–25.CrossRefGoogle Scholar
  87. Ogata, N., 1975, Ionic mechanisms of the depolarization shift in thin hippocampal slices, Exp. Neurol. 46:147–155.PubMedCrossRefGoogle Scholar
  88. Ogata, N., 1976, Mechanisms of the stereotyped high-frequency burst in hippocampal neurons in vitro, Brain Res. 103:386–388.CrossRefGoogle Scholar
  89. Ogata, N., Hori, N., and Katsuda, N., 1976, The correlation between extracellular potassium concentration and hippocampal epileptic activity in vitro, Brain Res. 110:371–375.PubMedCrossRefGoogle Scholar
  90. Oliver, A. P., Carman, J. S., Hoffer, B. J., and Wyatt, R. J., 1980a, Effect of altered calcium ion concentration on interictal spike generation in the hippocampal slice, Exp. Neurol. 68:489–499.PubMedCrossRefGoogle Scholar
  91. Oliver, A. P., Hoffer, B. J., and Wyatt, R. J., 1980b, Kindling induces long-lasting alterations in the responses of hippocampal neurons to elevated potassium levels in vitro, Science 208:1264–1265.PubMedCrossRefGoogle Scholar
  92. Prince, D. A., 1978, Neurophysiology of epilepsy, Annu. Rev. Neurosci. 1:395–415.PubMedCrossRefGoogle Scholar
  93. Prince, D. A., 1982, Epileptogenesis in hippocampal and neocortical neurons, in: Physiology and Pharmacology of Epileptogenic Phenomena (M. R. Klee, H. D. Lux, and E-J. Speckman, eds.), Raven Press, New York, pp. 151–161.Google Scholar
  94. Raabe, W. and Gumnit, R. J., 1975, Disinhibition in cat motor cortex by ammonia, J. Neurophysiol. 38:347–356.PubMedGoogle Scholar
  95. Ribak, C. E., Vaughn, J. E., and Saito, K., 1978, Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport, Brain Res. 140:315–332.PubMedCrossRefGoogle Scholar
  96. Robinson, J. H. and Deadwyler, S. A., 1981, Intracellular correlates of morphine excitation in the hippocampal slice preparation, Brain Res. 224:375–387.PubMedCrossRefGoogle Scholar
  97. Schmalbruch, H. and Jahnsen, H., 1981, Gap junctions on CA3 pyramidal cells of guinea pig hippocampus shown by freeze-fracture, Brain Res. 217:175–178.PubMedCrossRefGoogle Scholar
  98. Schneiderman, J. H. and Schwartzkroin, P. A., 1981, Evidence that penicillin-induced synchrony is not accompanied by increased electrotonic coupling, Neurosci. Abstr. 7:590.Google Scholar
  99. Schwartzkroin, P. A., 1975, Characteristics of CA1 neurons recorded intracellulary in the hippocampal slice, Brain Res. 85:423–435.PubMedCrossRefGoogle Scholar
  100. Schwartzkroin, P. A., 1977, Further characteristics of CA1 cells in vitro, Brain Res. 128:53–68.PubMedCrossRefGoogle Scholar
  101. Schwartzkroin, P. A. and Prince, D. A., 1978, Cellular and field potential properties of epileptogenic hippocampal slices, Brain Res. 147:117–130.PubMedCrossRefGoogle Scholar
  102. Schwartzkroin, P. A. and Prince, D. A., 1980a, Changes in excitatory and inhibitory synaptic potentials leading to epileptogenic activity, Brain Res. 183:61–76.PubMedCrossRefGoogle Scholar
  103. Schwartzkroin, P. A. and Prince, D. A., 1980b, Effects of TEA on hippocampal neurons, Brain Res. 185:169–181.PubMedCrossRefGoogle Scholar
  104. Schwartzkroin, P. A., and Slawksy, M. 1977, Probable calcium spikes in hippocampal neurons, Brain Res. 135:157–161.PubMedCrossRefGoogle Scholar
  105. Schwartzkroin, P. A. and Stafstrom, C. E., 1980, Effects of EGTA on the calcium activated afterhyperpolarization in hippocampal CA3 pyramidal cells, Science 210:1125–1126.PubMedCrossRefGoogle Scholar
  106. Schwartzkroin, P. A. and Wyler, M. D., 1980, Mechanisms underlying epileptiform burst discharge, Annu. Rev. Neurol. 7:95–107.CrossRefGoogle Scholar
  107. Siggins, G. R. and Zieglgansberger, W., 1981, Morphine and opioid peptides reduce inhibitory synaptic potentials in hippocampal pyramidal cells in vitro without alteration of membrane potential, Proc. Nat. Acad. Sci. USA 78:5230–5235.CrossRefGoogle Scholar
  108. Silfvenius, H., Olofsson, S., and Ridderheim, P-A., 1980, Induced epileptiform activity evoked from dendrites of hippocampal neurons, Acta Physiol. Scand. 108:109–111.PubMedCrossRefGoogle Scholar
  109. Spencer, W. A. and Kandel, E. R., 1961, Electrophysiology of hippocampal neurons. IV. Fast prepotentials, J. Neurophysiol. 24:272–284.Google Scholar
  110. Spencer, W. A. and Kandel, E. R., 1965, Synaptic inhibition in seizures, in: Basic Mechanisms of the Epilepsies (H. H. Jasper, A. A. Ward, Jr., and W. Pope, eds.), Little, Brown and Co., Boston, pp. 575–604.Google Scholar
  111. Storm-Mathisen, J., 1977, Localization of transmitter candidates in the brain: The hippocampal formation as a model, Prog. Neurobiol. 8:119–181.PubMedCrossRefGoogle Scholar
  112. Taylor, C. P. and Dudek, F. E., 1981, Physiological evidence for electrotonic coupling between CA1 pyramidal cells in rat hippocampal slices, Neurosci. Abstr. 7:519.Google Scholar
  113. Taylor, C. P., Dudek, F. E., 1982, Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses, Science 218:810–812.PubMedCrossRefGoogle Scholar
  114. Thalmann, R. H., 1982, Is the late hyperpolarization which follows synaptic stimulation of hippocampal pyramidal neurons calcium-dependent?, Neurosci. Abstr. 8:797.Google Scholar
  115. Thalmann, R. H. and Ayala, G. F., 1980, A picrotoxin-resistant hyperpolarizing response is elicited by orthodromic stimulation of hippocampal neurons, Neurosci. Abstr. 6:300.Google Scholar
  116. Thalmann, R. H., Peck, E. J., and Ayala, G. F., 1981, Biphasic response of hippocampal pyramidal neurons to GABA, Neurosci. Lett. 21:319–324.PubMedCrossRefGoogle Scholar
  117. Traub, R. D. and Wong, R. K. S., 1982, Cellular mechanism of neuronal synchronization in epilepsy, Science 216:745–747.PubMedCrossRefGoogle Scholar
  118. Traub, R. D. and Wong, R. K. S., 1983, Synchronized burst discharge in the disinhibited hippocampal slice. II. Model of the cellular mechanism, J. Neurophysiol. 49:459–471.PubMedGoogle Scholar
  119. Turner, D. A. and Schwartzkroin, P. A., 1980, Steady state analysis of intracellularly stained hippocampal neurons, J. Neurophysiol. 44:184–199.PubMedGoogle Scholar
  120. Urea, G., Frenk, H., Liebeskind, J. C., and Taylor, A. N., 1977, Morphine and enkephalin: Analgesic and epileptic properties, Science 197:83–86.CrossRefGoogle Scholar
  121. Valentino, R. J. and Dingledine, R., 1981, Presynaptic inhibitory effect of acetylcholine in the hippocampus, J. Neurosci. 1:784–792.PubMedGoogle Scholar
  122. Wong, R. K. S., 1982, Postsynaptic potentiation mechanism in the hippocampal pyramidal cells, in: Physiology and Pharmacology of Epileptogenic Phenomena (M. R. Klee, H. D. Lux and E.-J. Speckman, eds.), Raven Press, New York, pp. 163–173.Google Scholar
  123. Wong, R. K. S. and Prince, D. A., 1978, Participation of calcium spikes during intrinsic burst firing in hippocampal neurons, Brain Res. 159:385–390.PubMedCrossRefGoogle Scholar
  124. Wong, R. K. S. and Prince, D. A., 1979, Dendritic mechanisms underlying penicillin-induced epileptiform activity, Science 204:1228–1231.PubMedCrossRefGoogle Scholar
  125. Wong, R. K. S. and Prince, D. A., 1981, Afterpotential generation in hippocampal pyramidal cells, J. Neurophysiol. 45:86–97.PubMedGoogle Scholar
  126. Wong, R. K. S. and Traub, R. D., 1983, Synchronized burst discharge in the disinhibited hippocampal slice. I. Initiation in the CA2–CA3 region, J. Neurophysiol 49:442–458.PubMedGoogle Scholar
  127. Wong, R. K. S. and Watkins, D. J., 1982, Cellular factors influencing the GABA response in hippocampal pyramidal cells, J. Neurophysiol. 48:938–951.PubMedGoogle Scholar
  128. Wong, R. K. S., Prince, D. A., and Basbaum, A. I., 1979, Intradendritic recordings from hippocampal neurons, Proc. Nat. Acad. Sci. USA 76:986–990.PubMedCrossRefGoogle Scholar
  129. Yamamoto, C., 1972, Intracellular study of seizure-like afterdischarges elicited in thin hippocampal sections in vitro, Exp. Neurol. 35:154–164.CrossRefGoogle Scholar
  130. Yamamoto, C. and Kawai, N., 1968, Generation of the seizure discharge in thin sections from the guinea pig brain in chloride free medium in vitro, Jpn. J. Physiol. 18:620–631.PubMedCrossRefGoogle Scholar
  131. Zieglgansberger, W., French, E. D., Siggins, G. R., and Bloom, F. E., 1979, Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons, Science 205:415–417.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Bradley E. Alger
    • 1
  1. 1.Department of PhysiologyUniversity of Maryland School of MedicineBaltimoreUSA

Personalised recommendations