The EPSP-spike (E-S) component of long-term potentiation in the rat hippocampal slice is modulated by GABAergic but not cholinergic mechanisms

Long-term potentiation of synaptic efficacy (LTP) can be shown to consist of two components: a synaptic and an excitatory postsynaptic potential (EPSP)-spike (E-S) component. The E-S component is expressed as a leftward shift in the curve relating population spike amplitude as a function of EPSP slope. The participation of cholinergic and GABAergic processes in E-S potentiation was studied in field CA1 of rat hippocampal slices. Atropine, a muscarinic antagonist, did not prevent tetanus-induced E-S potentiation. The cholinergic agonist carbachol and the GABAA antagonist picrotoxin produced a leftward shift in the E-S relation; picrotoxin, but not carbachol, prevented the expression of tetanus-induced E-S potentiation. These observations indicate that an increase in the ratio of evoked excitation to inhibition and/or a reduction in tonic inhibition mediated by the activation of GABAA receptors contribute to E-S potentiation produced by high-frequency stimulation.

[1]  Y. Ben-Ari,et al.  Intracellular observations on the disinhibitory action of acetylcholine in the hippocampus , 1981, Neuroscience.

[2]  H. Wigström,et al.  Large long-lasting potentiation in the dentate gyrus in vitro during blockade of inhibition , 1983, Brain Research.

[3]  J. Taube,et al.  Mechanisms of long-term potentiation: EPSP/spike dissociation, intradendritic recordings, and glutamate sensitivity , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Storm-Mathisen.  Localization of transmitter candidates in the brain: the hippocampal formation as a model , 1977, Progress in Neurobiology.

[5]  G. V. Goddard,et al.  Septal modulation of the population spike in the fascia dentata produced by perforant path stimulation in the rat , 1982, Brain Research.

[6]  T. Bliss,et al.  Heterosynaptic changes accompany long‐term but not short‐term potentiation of the perforant path in the anaesthetized rat. , 1985, The Journal of physiology.

[7]  V. Vijayan.  Distribution of cholinergic neurotransmitter enzymes in the hippocampus and the dentate gyrus of the adult and the developing mouse , 1979, Neuroscience.

[8]  T. H. Brown,et al.  Conductance mechanism responsible for long-term potentiation in monosynaptic and isolated excitatory synaptic inputs to hippocampus. , 1986, Journal of neurophysiology.

[9]  W. Levy,et al.  Changes in translation of synaptic excitation to dentate granule cell discharge accompanying long-term potentiation. II. An evaluation of mechanisms utilizing dentate gyrus dually innervated by surviving ipsilateral and sprouted crossed temporodentate inputs. , 1981, Journal of neurophysiology.

[10]  R. Nicoll,et al.  Voltage clamp analysis of cholinergic action in the hippocampus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  P. Adams,et al.  Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. , 1986, Journal of neurophysiology.

[12]  J. Swann,et al.  Strontium supports synaptic transmission and long-lasting potentiation in the hippocampus , 1980, Brain Research.

[13]  R. Nicoll,et al.  Comparison of the action of baclofen with gamma‐aminobutyric acid on rat hippocampal pyramidal cells in vitro. , 1985, The Journal of physiology.

[14]  G. Somjen,et al.  Calcium dependance of synaptic transmission in the hippocampal slice , 1981, Brain Research.

[15]  R. Nicoll,et al.  Characterization of a slow cholinergic post‐synaptic potential recorded in vitro from rat hippocampal pyramidal cells. , 1984, The Journal of physiology.

[16]  J. Miller,et al.  Calcium-induced long-term potentiation in the hippocampus , 1982, Neuroscience.

[17]  S. Snyder,et al.  Cholinergic phosphatidylinositol modulation of inhibitory, G protein-linked neurotransmitter actions: electrophysiological studies in rat hippocampus. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[18]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[19]  T. Teyler,et al.  Long-term potentiation. , 1987, Annual review of neuroscience.

[20]  H. Wigström,et al.  Long‐term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea‐pig hippocampus. , 1987, The Journal of physiology.

[21]  K. Krnjević,et al.  Electrophysiological and pharmacological characteristics of facilitation of hippocampal population spikes by stimulation of the medial septum , 1982, Neuroscience.

[22]  C. Nyakas,et al.  Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus , 1987, Brain Research Bulletin.

[23]  P. Andersen,et al.  Possible mechanisms for long‐lasting potentiation of synaptic transmission in hippocampal slices from guinea‐pigs. , 1980, The Journal of physiology.

[24]  U. Frey,et al.  Calcium-induced long-term potentiation in the hippocampal slice: Characterization of the time course and conditions , 1986, Brain Research Bulletin.

[25]  C. Shute,et al.  Confirmation from choline acetylase analyses of a massive cholinergic innervation to the rat hippocampus , 1967, The Journal of physiology.

[26]  Paul R. Adams,et al.  Voltage-clamp analysis of muscarinic excitation in hippocampal neurons , 1982, Brain Research.