Generation of Theta and Gamma Rhythms in the Hippocampus

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Abstract

LEUNG L. S. Generation of theta and gamma rhythms in the hippocampus. NEUROSCI BIOBEHAV REV 22(2), 275–290, 1998.—In the behaving rat, theta rhythm was dominant during walking and rapid-eye-movement sleep, while irregular slow activity predominated during immobility and slow-wave sleep. Oscillatory evoked potentials of 20–50 Hz and spontaneous fast (gamma) waves were more prominent during theta compared with non-theta behaviors. The oscillations were simulated by a systems model with recurrent inhibition. The model also predicts a behaviorally dependent inhibition, which was confirmed experimentally using paired-pulse responses. Paired-pulse facilitation (PPF) of the population spikes in CA1 was larger during walking than immobility, mostly mediated by a cholinergic input. Spike responses in vitro were characterized by a relative lack of inhibition or disinhibition compared with the behaving rat. The two-input, two-dipole model of the theta rhythm in CA1 is reviewed. Afferents to the CA1 pyramidal cells are assumed to be rhythmic and consist of atropine-sensitive and atropine-resistant inputs driving the somata and distal dendrites, respectively. The atropine-sensitive theta rhythm was mainly caused by a series of Cl mediated inhibitory postsynaptic potentials (IPSPs) on pyramidal cells. It is suggested that previous claims of the participation of excitatory postsynaptic potentials (EPSPs) and not IPSPs in the intracellular recordings in vivo were flawed. Single cell recordings in vitro suggested that intrinsic voltage-dependent membrane potential oscillations modulate the response to a theta-frequency driving. Membrane potentials of pyramidal cells in vitro showed resonance in the theta frequency range.

Section snippets

HIPPOCAMPAL EEG VARIES WITH BEHAVIOR

VANDERWOLF [94]was the first to emphasize the correlation of the hippocampal EEG with the moment-to-moment behavior of the rat (Fig. 1). He stated that [94]

"Trains of rhythmical 6–12 Hz waves in the hippocampus and medial thalamus precede and accompany gross voluntary types of movement such as walking, rearing, jumping, etc. Behavioral immobility (in the alert state) and automatic movement patterns such as blinking, scratching, washing the face, licking or biting the fur, chewing food or lapping

EVOKED AND SPONTANEOUS OSCILLATIONS (20–50 Hz) IN THE HIPPOCAMPUS

When the Schaffer collaterals were stimulated by an electrical shock, a negative wave was observed in the apical dendrites of the CA1 pyramidal cells (Fig. 3); this negative wave reversed to a positive wave at the CA1 cell body layer. The apical dendritic negative wave was the population excitatory postsynaptic potential (EPSP). Increasing the stimulus intensity would induce a population spike, a synchronous firing of action potentials 3, 60, best seen at or near the cell body layer. Schaffer

PAIRED-PULSE RESPONSE IN CA1 AND DENTATE GYRUS

Austin et al. [6]found a robust behavioral dependence of paired-pulse responses in the dentate gyrus following medial perforant path stimulations. We [20]found a similar behavioral dependence of the paired-pulse responses in CA1 following Schaffer collaterals stimulation (Fig. 6). Paired-pulses probe a system in a way that a single pulse could not. The second of a pair of pulses tests the excitability of the neurons at various delays (interpulse intervals, IPIs) after the first pulse perturbs

TEMPERATURE EFFECT ON HIPPOCAMPAL EEG AND EVOKED POTENTIALS

Recent experiments suggest that part of the change of hippocampal extracellular potentials may be mediated by a change in brain temperature 2, 78. Most of the physiological measures reviewed here varied with the moment-to-moment behavior of the rat, much faster than could be accounted for by the slow change in brain temperature during muscle activity. Presumably, brain temperature during walking should not differ before and after atropine, and yet the evoked potential oscillation and PPF of

THETA RHYTHM IN VIVO: EVIDENCE FOR IPSPS AND EPSPS

In anesthetized animals, the theta rhythm showed amplitude peaks at the stratum oriens and stratum radiatum, with an abrupt phase reversal (180°) near the pyramidal cell layer 12, 34. Fox and Ranck 28, 82and Buzsaki et al. [18]have provided evidence that putative interneurons are driven rhythmically at a theta frequency. Artemenko [5]and Fox et al. [29]have provided some evidence that IPSPs participate in an intracellular theta rhythm. The laminar profile of the antidromically evoked IPSP field

THETA RHYTHM IN VIVO: EXTRACELLULAR PROFILE AND MODEL

Theta rhythm in the behaving rat was inferred to consist of atropine-sensitive and atropine-resistant components 10, 46, 95. The atropine-sensitive component is likely mediated by the cholinergic afferents from the medial septal area while the atropine-resistant component is suggested to be mediated by serotonergic afferents from the raphe [96]. Instead of an abrupt phase shift of the theta rhythm in proximal stratum radiatum of urethane-anesthetized [12]or curarized rats [106], Winson [105]

THETA RHYTHM GENERATION IN VITRO

The hippocampal slice in vitro, with normal artificial cerebrospinal fluid, had little spontaneous activity. Konopacki et al. ([43]; reviewed in [11]) first demonstrated that perfusion of carbachol induced periods of theta-frequency oscillations in the hippocampus in vitro. This was confirmed by MacVicar and Tse [75]in CA3, who also showed that the carbachol-induced rhythm in vitro was apparently synaptically generated, and that it could be abolished by tetrodotoxin [75]. Carbachol may induce

Acknowledgements

I thank the Natural Sciences and Engineering Research Council of Canada for continuous support of this research. Through the years, some support was also provided by NS-25383 from the National Institutes of Health (USA), Medical Research Council (Canada) and the Physicians Services Incorporated (Ontario). Important data were originally collected by associates and students: A. Au, C. Yim, H. W. Yu and D. Zhao (in vitro), K. Canning, L. Roth, C. Yim and K. Wu (in anesthetized rats) and F. Cao, C.

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