Ultra-slow oscillation (0.025 Hz) triggers hippocampal afterdischarges in Wistar rats

doi:10.1016/S0306-4522(99)00367-X

Neuroscience

Volume 94, Issue 3, October 1999, Pages 735-743

https://doi.org/10.1016/S0306-4522(99)00367-X Get rights and content

Abstract

Oscillations in neuronal networks are assumed to serve various physiological functions, from coordination of motor patterns to perceptual binding of sensory information. Here, we describe an ultra-slow oscillation (0.025 Hz) in the hippocampus. Extracellular and intracellular activity was recorded from the CA1 and subicular regions in rats of the Wistar and Sprague–Dawley strains, anesthetized with urethane. In a subgroup of Wistar rats (23%), spontaneous afterdischarges (4.7±1.6 s) occurred regularly at 40.8±15.7 s. The afterdischarge was initiated by a fast increase of population synchrony (100–250 Hz oscillation; “tonic” phase), followed by large-amplitude rhythmic waves and associated action potentials at gamma and beta frequency (15–50 Hz; “clonic” phase). The afterdischarges were bilaterally synchronous and terminated relatively abruptly without post-ictal depression. Single-pulse stimulation of the commissural input could trigger afterdischarges, but only at times when they were about to occur. Commissural stimulation evoked inhibitory postsynaptic potentials in pyramidal cells. However, when the stimulus triggered an afterdischarge, the inhibitory postsynaptic potential was absent and the cells remained depolarized during most of the afterdischarge. Afterdischarges were not observed in the Sprague–Dawley rats. Long-term analysis of interneuronal activity in intact, drug-free rats also revealed periodic excitability changes in the hippocampal network at 0.025 Hz.

These findings indicate the presence of an ultra-slow oscillation in the hippocampal formation. The ultra-slow clock induced afterdischarges in susceptible animals. We hypothesize that a transient failure of GABAergic inhibition in a subset of Wistar rats is responsible for the emergence of epileptiform patterns.

Section snippets

Experimental procedures

The experiments were performed on 73 Wistar (HsdBrlHan : WIST; National Laboratory Animal Center, University of Kuopio, Kuopio, Finland) and 45 Sprague–Dawley (Hilltop, Scottsdale, PA, USA) male rats (180–260 g). All efforts were made to minimize animal suffering, to reduce the number of animals used and to utilize alternatives to in vivo techniques. The recording methods were described in detail earlier.20., 35. In brief, rats were anesthetized with an intraperitoneal injection of urethane

Ultra-slow oscillation in the hippocampus

Hippocampal activity in the anesthetized rat consists of various irregular field potentials and oscillations.20., 21., 34., 35., 42., 61., 62. Deep anesthesia is characterized by large-amplitude, low-frequency oscillation (0.5–1 Hz, slow delta waves; Fig. 1A), associated with phase-locked discharges of multiple unit activity. Superimposed on this slow rhythm, lower amplitude, faster waves in the gamma (30–100 Hz) and beta (10–30 Hz) are typically present, similar to the delta-modulated gamma

Discussion

The novel findings of the present experiments are (i) the presence of an ultra-slow oscillatory pattern (0.025 Hz) in the hippocampal formation, and (ii) the occurrence of spontaneous afterdischarges in a subgroup of rats of the Wistar strain. These spontaneous afterdischarge episodes were triggered by the ultra-slow cyclic increases of network excitability.

Acknowledgements

This work was supported by the Academy of Finland (32391) and the NIH (NS34994, MH54671).

References (63)

P Achermann et al.
Low-frequency (<1 Hz) oscillations in the human sleep electroencephalogram
Neuroscience
(1997)
Y Ben-Ari
Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy
Neuroscience
(1985)
G Buzsaki et al.
Petit mal epilepsy and parkinsonian tremor: hypothesis of a common pacemaker
Neuroscience
(1990)
J Csicsvari et al.
Reliability and state dependence of pyramidal cell–interneuron synapses in the hippocampus: an ensemble approach in the behaving rat
Neuron
(1998)
G Jando et al.
Spike-and-wave epilepsy in rats: sex differences and inheritance of physiological traits
Neuroscience
(1995)
J.G Jefferys et al.
Neuronal networks for induced `40 Hz' rhythms
Trends Neurosci.
(1996)
A Mason
Electrophysiology and burst-firing of rat subicular pyramidal neurons in vitro: a comparison with area CA1
Brain Res.
(1993)
J.L Noebels
Targeting epilepsy genes
Neuron
(1996)
R.J Racine
Modification of seizure activity by electrical stimulation: cortical areas
Electroenceph. clin. Neurophysiol.
(1975)
P Andersen et al.
Lamellar organization of hippocampal excitatory pathways
Acta physiol. scand.
(1969)

L.S Benardo

Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro

J. Physiol.

(1994)

R Bianchi et al.

Carbachol-induced synchronized rhythmic bursts in CA3 neurons of guinea pig hippocampus in vitro

J. Neurophysiol.

(1994)

A Bragin et al.

Epileptic afterdischarge in the hippocampal–entorhinal system: current source density and unit studies

Neuroscience

(1997)

A Bragin et al.

Termination of epileptic afterdischarge in the hippocampus

J. Neurosci.

(1997)

B.W Connors et al.

Two inhibitory postsynaptic potentials, and GABA_A and GABA_B receptor-mediated responses in neocortex of rat and cat

J. Physiol.

(1988)

A.V Delgado-Escueta et al.

Progress in mapping human epilepsy genes

Epilepsia

(1994)

C.T Dickson et al.

Muscarinic induction of synchronous population activity in the entorhinal cortex

J. Neurosci.

(1997)

Engel J. J. (1989) Seizures and Epilepsy. F. A. Davis,...

E.V Golanov et al.

Spontaneous waves of cerebral blood flow associated with a pattern of electrocortical activity

Am. J. Physiol.

(1994)

C.M Gray

Synchronous oscillations in neuronal systems: mechanisms and functions

J. comput. Neurosci.

(1994)

D.A Hosford et al.

The role of GABA_B receptor activation in absence seizures of lethargic (lh/lh) mice

Science

(1992)

P.C Jobe et al.

Scope and contribution of genetic models to an understanding of the epilepsies

Crit. Rev. Neurobiol.

(1991)

A Kamondi et al.

Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus

J. Neurosci.

(1998)

A Kamondi et al.

Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials

Hippocampus

(1998)

A Kandel et al.

Cellular–synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat

J. Neurosci.

(1997)

U Kim et al.

Functional dynamics of GABAergic inhibition in the thalamus

Science

(1997)

L.S Leung

Fast (beta) rhythms in the hippocampus: a review

Hippocampus

(1992)

L.S Leung et al.

Long-lasting effects of partial hippocampal kindling on hippocampal physiology and function

Hippocampus

(1994)

R.R Llinas

The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function

Science

(1988)

B.A MacVicar et al.

Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices

J. Physiol.

(1989)

C Marescaux et al.

Genetic absence epilepsy in rats from Strasbourg—a review

J. neural Transm., Suppl.

(1992)

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Ultra-slow oscillation (0.025 Hz) triggers hippocampal afterdischarges in Wistar rats

Abstract

Section snippets

Experimental procedures

Ultra-slow oscillation in the hippocampus

Discussion

Acknowledgements

Neuroscience

Neuroscience

Neuroscience

Neuron

Neuroscience

Trends Neurosci.

Brain Res.

Neuron

Electroenceph. clin. Neurophysiol.

Lamellar organization of hippocampal excitatory pathways

Acta physiol. scand.

Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro

J. Physiol.

Carbachol-induced synchronized rhythmic bursts in CA3 neurons of guinea pig hippocampus in vitro

J. Neurophysiol.

Epileptic afterdischarge in the hippocampal–entorhinal system: current source density and unit studies

Neuroscience

Termination of epileptic afterdischarge in the hippocampus

J. Neurosci.

Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat

J. Physiol.

Progress in mapping human epilepsy genes

Epilepsia

Muscarinic induction of synchronous population activity in the entorhinal cortex

J. Neurosci.

Spontaneous waves of cerebral blood flow associated with a pattern of electrocortical activity

Am. J. Physiol.

Synchronous oscillations in neuronal systems: mechanisms and functions

J. comput. Neurosci.

The role of GABAB receptor activation in absence seizures of lethargic (lh/lh) mice

Science

Scope and contribution of genetic models to an understanding of the epilepsies

Crit. Rev. Neurobiol.

Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus

J. Neurosci.

Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials

Hippocampus

Cellular–synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat

J. Neurosci.

Functional dynamics of GABAergic inhibition in the thalamus

Science

Fast (beta) rhythms in the hippocampus: a review

Hippocampus

Long-lasting effects of partial hippocampal kindling on hippocampal physiology and function

Hippocampus

The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function

Science

Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices

J. Physiol.

Genetic absence epilepsy in rats from Strasbourg—a review

J. neural Transm., Suppl.

Two inhibitory postsynaptic potentials, and GABA_A and GABA_B receptor-mediated responses in neocortex of rat and cat

The role of GABA_B receptor activation in absence seizures of lethargic (lh/lh) mice