Glutamatergic synaptic transmission participates in generating the hippocampal EEG

The participation of ionotropic glutamatergic synapses in the generation of hippocampal electroencephalography (EEG) of behaving rats has not been systematically studied. In this study, field potentials in hippocampal CA1 were recorded following injection of N‐methyl‐D‐aspartate (NMDA) and α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid (AMPA) receptor antagonists, or vehicle control, either into the lateral ventricles or directly into the hippocampus or the medial septum. Intraventricular (i.c.v.) AMPA receptor antagonist 6,7‐dinitroquinoxaline‐2,3,dione (DNQX, 5–10 μg) decreased the commissural evoked potential and the amplitude of the hippocampal EEG, including the theta rhythm. Theta frequency was decreased by 10 μg, but not 5 μg DNQX i.c.v. Unilateral intrahippocampal injection of DNQX (5 μg) only decreased the amplitude, but not the frequency, of the theta rhythm near the site of injection, without affecting theta amplitude or frequency at the opposite hippocampus. Other than theta, the large irregular activity (with a delta frequency peak at 1–2 Hz) and gamma EEG (30–100 Hz) were also decreased by i.c.v. and intrahippocampal injections of DNQX. Intrahippocampal injection of NMDA receptor antagonist D‐2‐amino‐5‐phosphonovaleric acid (D‐APV, 2.5 μg) decreased the amplitude of the theta rhythm and, less consistently, the gamma EEG. The frequency of the theta rhythm and the peak of the commissural evoked potential were not significantly affected by intrahippocampal D‐APV injection. Medial septal injections of D‐APV or D,L‐APV (2.24 μg in 0.4 μl), but not DNQX (10 μg in 0.4 μl), decreased the amplitude of the hippocampal theta significantly, but theta frequency was not significantly affected. It is concluded that both NMDA and AMPA receptors in the hippocampus are involved in generating the amplitude of the hippocampal EEG of theta and gamma frequencies, while NMDA receptors in the medial septum are involved in controlling the amplitude of theta and gamma EEG in the hippocampus. Excitatory glutamatergic synaptic currents, activated by afferents from the entorhinal cortex and CA3, are suggested to participate in hippocampal EEG activities. © 2004 Wiley‐Liss, Inc.

[1]  G. Buzsáki,et al.  Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. , 1996, The Journal of physiology.

[2]  Liang Zhang,et al.  A fundamental oscillatory state of isolated rodent hippocampus , 2002, The Journal of physiology.

[3]  B. Bland,et al.  Intraseptal procaine abolishes hypothalamic stimulation-induced wheel- running and hippocampal theta field activity in rats , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  C. H. Vanderwolf,et al.  Hippocampal rhythmical slow activity following ibotenic acid lesions of the septal region. I. Relations to behavior and effects of atropine and urethane , 1987, Brain Research.

[5]  R. Traub,et al.  Neuronal Networks of the Hippocampus , 1991 .

[6]  L. Leung Theta rhythm during REM sleep and waking: correlations between power, phase and frequency. , 1984, Electroencephalography and clinical neurophysiology.

[7]  Richard T. Marrocco,et al.  Arousal systems , 1994, Current Opinion in Neurobiology.

[8]  U. Frey,et al.  Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  C. Léránth,et al.  A Population of Supramammillary Area Calretinin Neurons Terminating on Medial Septal Area Cholinergic and Lateral Septal Area Calbindin-Containing Cells Are Aspartate/Glutamatergic , 1996, The Journal of Neuroscience.

[10]  H. Bokor,et al.  Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [3H]D-aspartate labelling and immunocytochemistry , 2002, Neuroscience.

[11]  I. Whishaw,et al.  Release of acetylcholine from the hippocampus of freely moving rats during sensory stimulation and running , 1979, Neuropharmacology.

[12]  B. Everitt,et al.  The Distribution of Neurons Coexpressing Immunoreactivity to AMPA‐sensitive Glutamate Receptor Subtypes (GluR1‐4) and Nerve Growth Factor Receptor in the Rat Basal Forebrain , 1995, The European journal of neuroscience.

[13]  B. H. Bland The physiology and pharmacology of hippocampal formation theta rhythms , 1986, Progress in Neurobiology.

[14]  T. Dunwiddie,et al.  Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[16]  C. Trepel,et al.  Intraseptal Microinfusion of Muscimol: Effects on Hippocampal Formation Theta Field Activity and Phasic Theta-ON Cell Discharges , 1996, Experimental Neurology.

[17]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[19]  A. Heynen,et al.  Effects of perforant path procaine on hippocampal type 2 rhythmical slow‐wave activity (theta) in the urethane‐anesthetized rat , 1994, Hippocampus.

[20]  G. Buzsáki,et al.  Interdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis , 1999, The Journal of Neuroscience.

[21]  D. J. Stewart,et al.  Hippocampal theta rhythm in behaving rats following ibotenic acid lesion of the septum , 1994, Hippocampus.

[22]  B. Shen,et al.  N‐methyl‐D‐aspartate receptor antagonists are less effective in blocking long‐term potentiation at apical than basal dendrites in hippocampal CA1 of awake rats , 1999, Hippocampus.

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

[24]  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.

[25]  C. H. Vanderwolf Cerebral activity and behavior: control by central cholinergic and serotonergic systems. , 1988, International review of neurobiology.

[26]  I. Izquierdo,et al.  Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. , 1992, Behavioral and neural biology.

[27]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[28]  J. Rawlins,et al.  Septo-hippocampal connections and the hippocampal theta rhythm , 1979, Experimental Brain Research.

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

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

[31]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[32]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[33]  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.

[34]  L. Leung Pharmacology of theta phase shift in the hippocampal CA1 region of freely moving rats. , 1984, Electroencephalography and clinical neurophysiology.

[35]  T. Bliss,et al.  NMDA Receptors May Be Involved in Generation of Hippocampal Theta Rhythm , 1988 .

[36]  S. Fox,et al.  Intracellular recordings from medial septal neurons during hippocampal theta rhythm , 1997, Experimental Brain Research.

[37]  Y Fujita,et al.  INTRACELLULAR RECORDS FROM HIPPOCAMPAL PYRAMIDAL CELLS IN RABBIT DURING THETA RHYTHM ACTIVITY. , 1964, Journal of neurophysiology.

[38]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

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

[40]  J. Kauer,et al.  Properties of carbachol-induced oscillatory activity in rat hippocampus. , 1997, Journal of neurophysiology.

[41]  M. Hasselmo,et al.  NMDA-dependent modulation of CA1 local circuit inhibition , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Fiona E. N. LeBeau,et al.  A model of gamma‐frequency network oscillations induced in the rat CA3 region by carbachol in vitro , 2000, The European journal of neuroscience.

[43]  J. Winson Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. , 1978, Science.

[44]  A. Heynen,et al.  Induction of RSA-like oscillations in both the in-vitro and in-vivo hippocampus. , 1991, Neuroreport.

[45]  T. Sejnowski,et al.  Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5–2 Hz), theta (5–12 Hz), and gamma (35–70 Hz) bands , 2000, Hippocampus.

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

[47]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  Jan Konopacki,et al.  Relationship between membrane potential oscillations and rhythmic discharges in identified hippocampal theta-related cells. , 2002, Journal of neurophysiology.

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

[50]  John H. Martin Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat , 1991, Neuroscience Letters.

[51]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

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

[53]  A. Alonso,et al.  Rhythmically discharging basal forebrain units comprise cholinergic, GABAergic, and putative glutamatergic cells. , 2003, Journal of neurophysiology.

[54]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[55]  S. Fox Membrane potential and impedance changes in hippocampal pyramidal cells during theta rhythm , 2004, Experimental Brain Research.

[56]  Lucia Wittner,et al.  Simultaneous activation of gamma and theta network oscillations in rat hippocampal slice cultures , 2002, The Journal of physiology.

[57]  B. MacVicar,et al.  Theta-frequency facilitation of AMPA receptor-mediated synaptic currents in the principal cells of the medial septum. , 2001, Journal of neurophysiology.

[58]  C. Léránth,et al.  Muscarinic Tone Sustains Impulse Flow in the Septohippocampal GABA But Not Cholinergic Pathway: Implications for Learning and Memory , 2000, The Journal of Neuroscience.

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

[60]  C. Stumpf,et al.  Drug action on the electrical activity of the hippocampus. , 1965, International review of neurobiology.

[61]  I. Kirk Frequency Modulation of Hippocampal Theta by the Supramammillary Nucleus, and Other Hypothalamo–Hippocampal Interactions: Mechanisms and Functional Implications , 1998, Neuroscience & Biobehavioral Reviews.

[62]  L. Leung,et al.  Spectral analysis of hippocampal EEG in the freely moving rat: effects of centrally active drugs and relations to evoked potentials. , 1985, Electroencephalography and clinical neurophysiology.

[63]  Stan Leung Lai-Wo Pharmacology of theta phase shift in the hippocampal CA1 region of freely moving rats , 1984 .

[64]  T. Kaibara,et al.  Basal versus apical dendritic long-term potentiation of commissural afferents to hippocampal CA1: a current-source density study , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  J. Winson,et al.  Patterns of hippocampal theta rhythm in the freely moving rat. , 1974, Electroencephalography and clinical neurophysiology.

[66]  L. S. Leung,et al.  Nonlinear feedback model of neuronal populations in hippocampal CAl region. , 1982, Journal of neurophysiology.

[67]  Fiona E. N. LeBeau,et al.  A Model of Atropine‐Resistant Theta Oscillations in Rat Hippocampal Area CA1 , 2002, The Journal of physiology.

[68]  J. Bizot,et al.  Hippocampal theta rhythm in anesthetized rats: role of AMPA glutamate receptors. , 1999, Neuroreport.

[69]  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.

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

[71]  W. Seifert Neurobiology of the hippocampus , 1983 .

[72]  L. Bianchi,et al.  Glutamatergic Modulation of Cortical Acetylcholine Release in the Rat: A Combined In Vivo Microdialysis, Retrograde Tracing and lmmunohistochemical Study , 1997, The European journal of neuroscience.

[73]  H. Bokor,et al.  The supramammillo-hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: a combined [3H]d-aspartate autoradiographic and immunohistochemical study , 2000, Neuroscience.

[74]  Jingyi Ma,et al.  The Septohippocampal System Participates in General Anesthesia , 2002, The Journal of Neuroscience.

[75]  F. H. Lopes da Silva,et al.  Spectral characteristics of the hippocampal EEG in the freely moving rat. , 1982, Electroencephalography and clinical neurophysiology.

[76]  Roger D. Traub,et al.  Simulation of Gamma Rhythms in Networks of Interneurons and Pyramidal Cells , 1997, Journal of Computational Neuroscience.

[77]  R. Vertes,et al.  Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. , 1997, Neuroscience.

[78]  L STAN LEUNG,et al.  Generation of Theta and Gamma Rhythms in the Hippocampus , 1998, Neuroscience & Biobehavioral Reviews.

[79]  M. Stewart,et al.  Do septal neurons pace the hippocampal theta rhythm? , 1990, Trends in Neurosciences.

[80]  G. Buzsáki,et al.  Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity‐dependent phase‐precession of action potentials , 1998, Hippocampus.

[81]  S. J. Martin,et al.  Reversible neural inactivation reveals hippocampal participation in several memory processes , 1999, Nature Neuroscience.

[82]  I. Kirk,et al.  Evidence for Differential Control of Posterior Hypothalamic, Supramammillary, and Medial Mammillary Theta-Related Cellular Discharge by Ascending and Descending Pathways , 1996, The Journal of Neuroscience.

[83]  C. H. Vanderwolf,et al.  Hippocampal EEG and behavior: changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. , 1973, Behavioral biology.

[84]  P. Monmaur,et al.  Intraseptal infusion of selective and competitive glutamate receptor agonist NMDA and antagonist d-2-amino-5-phosphonopentanoic acid spectral implications for the physostigmine-induced hippocampal theta rhythm in urethane-anesthetized rats , 1996, Experimental Brain Research.

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

[86]  G. Lynch,et al.  Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. , 1988, Science.

[87]  W B Levy,et al.  Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. , 1992, Journal of neurophysiology.

[88]  Lai-Wo Stan Leung,et al.  APV, an N-methyl-d-aspartate receptor antagonist, blocks the hippocampal theta rhythm in behaving rats , 1988, Brain Research.

[89]  Jingyi Ma,et al.  Metabotropic glutamate receptors in the hippocampus and nucleus accumbens are involved in generating seizure-induced hippocampal gamma waves and behavioral hyperactivity , 2002, Behavioural Brain Research.