Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare.

The ionic conductances underlying membrane potential oscillations of hippocampal CA1 interneurons located near the border between stratum lacunosum-moleculare and stratum radiatum (LM) were investigated using whole cell current-clamp recordings in rat hippocampal slices. At 22 degrees C, when LM cells were depolarized near spike threshold by current injection, 91% of cells displayed 2-5 Hz oscillations in membrane potential, which caused rhythmic firing. At 32 degrees C, mean oscillation frequency increased to 7.1 Hz. Oscillations were voltage dependent and were eliminated by hyperpolarizing cells 6-10 mV below spike threshold. Blockade of ionotropic glutamate and GABA synaptic transmission did not affect oscillations, indicating that they were not synaptically driven. Oscillations were eliminated by tetrodotoxin, suggesting that Na+ currents generate the depolarizing phase of oscillations. Oscillations were not affected by blocking Ca2+ currents with Cd2+ or Ca2+-free ACSF or by blocking the hyperpolarization-activated current (Ih) with Cs+. Both Ba2+ and a low concentration of 4-aminopyridine (4-AP) reduced oscillations but TEA did not. Theta-frequency oscillations were much less common in interneurons located in stratum oriens. Intrinsic membrane potential oscillations in LM cells of the CA1 region thus involve an interplay between inward Na+ currents and outward K+ currents sensitive to Ba2+ and 4-AP. These oscillations may participate in rhythmic inhibition and synchronization of pyramidal neurons during theta activity in vivo.

[1]  Michael Frotscher,et al.  Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study , 1985, The Journal of comparative neurology.

[2]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. , 1988, Brain research.

[3]  M. Yeckel,et al.  Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Lacaille,et al.  Ultrastructure of stratum lacunosum moleculare interneurons of hippocampal CA1 region , 1988, Synapse.

[5]  T. Freund,et al.  Innervation of different peptide-containing neurons in the hippocampus by gabaergic septal afferents , 1990, Neuroscience.

[6]  C. McBain,et al.  The hyperpolarization‐activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens‐alveus interneurones. , 1996, The Journal of physiology.

[7]  Y. Ben‐Ari,et al.  Hippocampal CA1 lacunosum-moleculare interneurons: modulation of monosynaptic GABAergic IPSCs by presynaptic GABAB receptors. , 1995, Journal of neurophysiology.

[8]  M. Frotscher,et al.  Cholinergic innervation of hippocampal GAD‐ and somatostatin‐immunoreactive commissural neurons , 1987, The Journal of comparative neurology.

[9]  G. Buzsáki,et al.  Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells , 1995, Hippocampus.

[10]  L W Leung,et al.  Model of gradual phase shift of theta rhythm in the rat. , 1984, Journal of neurophysiology.

[11]  B. H. Bland,et al.  Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex , 1993, Progress in Neurobiology.

[12]  P. Schwartzkroin,et al.  Effects of cholinergic agonists on immature rat hippocampal neurons. , 1991, Brain research. Developmental brain research.

[13]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

[14]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[15]  F. W. Tse,et al.  Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices. , 1989, The Journal of physiology.

[16]  A. Alonso,et al.  Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. , 1997, Journal of neurophysiology.

[17]  J. Behrends,et al.  Cholinergic modulation of synaptic inhibition in the guinea pig hippocampus in vitro: excitation of GABAergic interneurons and inhibition of GABA-release. , 1993, Journal of neurophysiology.

[18]  J. B. Ranck,et al.  Generation of theta rhythm in medial entorhinal cortex of freely moving rats , 1980, Brain Research.

[19]  P. Schwartzkroin,et al.  Effects of temperature alterations on population and cellular activities in hippocampal slices from mature and immature rabbit , 1988, Brain Research.

[20]  G. Lynch,et al.  Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation , 1986, Brain Research.

[21]  M. Bruce MacIver,et al.  Carbachol-induced EEG ‘theta’ activity in hippocampal brain slices , 1987, Brain Research.

[22]  M. Atzori Pyramidal cells and stratum lacunosum‐moleculare interneurons in the CA1 hippocampal region share a GABAergic spontaneous input , 1996, Hippocampus.

[23]  J. Lisman,et al.  Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro , 1995, Neuron.

[24]  L. Kellényi,et al.  Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: Current-source density analysis, effects of urethane and atropine , 1986, Brain Research.

[25]  Matthew I. Banks,et al.  The Synaptic Basis of GABAA,slow , 1998, The Journal of Neuroscience.

[26]  Roland S. G. Jones Entorhinal-hippocampal connections: a speculative view of their function , 1993, Trends in Neurosciences.

[27]  R. Llinás,et al.  Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II , 1989, Nature.

[28]  W. Levy,et al.  Ultrastructural identification of entorhinal cortical synapses in CA1 stratum lacunosum‐moleculare of the rat , 1994, Hippocampus.

[29]  C. Y. Yim,et al.  Intrinsic membrane potential oscillations in hippocampal neurons in vitro , 1991, Brain Research.

[30]  A. Alonso,et al.  Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. , 1993, Journal of neurophysiology.

[31]  P. Schwartzkroin,et al.  Physiological and morphological identification of a nonpyramidal hippocampal cell type , 1978, Brain Research.

[32]  C. McBain,et al.  Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons , 1996, The Journal of Neuroscience.

[33]  Lai-Wo S. Leung,et al.  Intracellular records of theta rhythm in hippocampal CA1 cells of the rat , 1986, Brain Research.

[34]  D. Prince,et al.  Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CA1 neurons in vitro , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  J. Lacaille,et al.  Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro , 1990, Neuroscience.

[36]  R. Racine,et al.  Piriform cortex efferents to the entorhinal cortex in vivo: kindling‐induced potentiation and the enhancement of long‐term potentiation by low‐frequency piriform cortex or medial septal stimulation , 1997, Hippocampus.

[37]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[38]  P. Somogyi,et al.  Unitary IPSPs evoked by interneurons at the stratum radiatum‐stratum lacunosum‐moleculare border in the CA1 area of the rat hippocampus in vitro , 1998, The Journal of physiology.

[39]  J. Storm Potassium currents in hippocampal pyramidal cells. , 1990, Progress in brain research.

[40]  D. Prince,et al.  Anomalous inward rectification in hippocampal neurons. , 1979, Journal of neurophysiology.

[41]  J. Lacaille,et al.  Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. , 1996, Journal of neurophysiology.

[42]  D. McCormick,et al.  Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h). , 1997, Journal of neurophysiology.

[43]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[44]  M. Stewart,et al.  Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators , 1993, Brain Research.

[45]  R. Llinás,et al.  Electrophysiology of the mammillary complex in vitro. II. Medial mammillary neurons. , 1992, Journal of neurophysiology.

[46]  D. D. Fraser,et al.  Low-threshold transient calcium current in rat hippocampal lacunosum- moleculare interneurons: kinetics and modulation by neurotransmitters , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  T. Freund,et al.  GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus , 1988, Nature.

[48]  M. Deschenes,et al.  Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. , 1993, Journal of neurophysiology.

[49]  J. Lacaille,et al.  Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[51]  J. Lacaille,et al.  Properties of unitary IPSCs in hippocampal pyramidal cells originating from different types of interneurons in young rats. , 1997, Journal of neurophysiology.

[52]  Menno P. Witter,et al.  Entorhinal projections to the hippocampal CA1 region in the rat: An underestimated pathway , 1988, Neuroscience Letters.

[53]  Two temporally overlapping "delayed-rectifiers" determine the voltage-dependent potassium current phenotype in cultured hippocampal interneurons. , 1996, Journal of neurophysiology.

[54]  Model Synapses with Frequency Potentiation Characteristics Can Cooperatively Enhance Hebbian Learning , 1995 .

[55]  A Núñez,et al.  Intracellular theta-rhythm generation in identified hippocampal pyramids. , 1987, Brain research.

[56]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm , 1988, Brain Research.

[57]  O. Steward,et al.  Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  H. Petsche,et al.  [The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells]. , 1962, Electroencephalography and clinical neurophysiology.

[59]  I. Módy,et al.  Synaptic Communication among Hippocampal Interneurons: Properties of Spontaneous IPSCs in Morphologically Identified Cells , 1997, The Journal of Neuroscience.

[60]  R. Llinás,et al.  Ionic basis for the electro‐responsiveness and oscillatory properties of guinea‐pig thalamic neurones in vitro. , 1984, The Journal of physiology.

[61]  T. Freund,et al.  Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. , 1997, The Journal of physiology.

[62]  Pankaj Sah,et al.  Ca2+-activated K+ currents in neurones: types, physiological roles and modulation , 1996, Trends in Neurosciences.

[63]  J. Lacaille,et al.  Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  W. Bun˜o,et al.  Intracellular θ-rhythm generation in identified hippocampal pyramids , 1987, Brain Research.

[65]  C. McBain,et al.  Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region , 1995, Neuron.

[66]  J. Lacaille,et al.  Membrane properties and synaptic responses of interneurons located near the stratum lacunosum-moleculare/radiatum border of area CA1 in whole-cell recordings from rat hippocampal slices. , 1994, Journal of neurophysiology.