A fundamental oscillatory state of isolated rodent hippocampus

Abstract

Population neuronal rhythms of various frequencies are observed in the rodent hippocampus during distinct behavioural states. However, the question of whether the hippocampus exhibits properties of spontaneous rhythms and population synchrony in isolation has not been definitively answered. To address this, we developed a novel preparation for studying neuronal rhythms in a relatively large hippocampal tissue in vitro. We isolated the whole hippocampus from mice up to 28 days postnatal age, removing the dentate gyrus while preserving the functional CA3‐to‐CA1 connections. Placing the hippocampal isolate in a perfusion chamber for electrophysiological assessment extracellular recordings from the CA1 revealed rhythmic field potential of 0.5 to ≤ 4 Hz that occurred spontaneously and propagated along the ventro‐dorsal hippocampal axis. We provide convergent evidence, via measurements of extracellular pH and K+, recordings of synaptic and intracellular activities and morphological assessments, verifying that these rhythms were not the consequence of hypoxia. Data obtained via simultaneous extracellular and patch clamp recordings suggest that the spontaneous rhythms represent a summation of GABAergic IPSPs originating from pyramidal neurons, which result from synchronous discharges of GABAergic inhibitory interneurons. Similar spontaneous field rhythms were also observed in the hippocampal isolate prepared from young gerbils and rats. Based on these data, we postulate that the spontaneous rhythms represent a fundamental oscillatory state of the hippocampal circuitry isolated from extra‐hippocampal inputs.

Endogenous Waves in Hippocampal Slices

“…Endogenous SPWs have not previously been described in vitro, probably because slices are usually prepared from more rostral segments of the hippocampus where the dense associational connectivity of CA3 is less likely to be preserved within a 350-m slice. Consistent with this idea, spontaneous slow EEG patterns have been reported in studies using mouse hippocampal slices cut at thicknesses Ն500 m (Wu et al 2002;Yanovsky et al 1995), increasing the likelihood that CA3 axon collaterals will remain within the plane of the slice. Other factors such as the use of interface chambers as opposed to submerged slices and the ratio of calcium to magnesium in recording ACSF may also be important for detection of this activity.…”

Synaptic plasticity in early aging

“…Importantly, memory in the first (rapid, basal) component appears to not consolidate while that in the second (gradual, apical) does, suggesting that the former, but not the latter, is unstable. Pertinent to this, the hippocampus and cortex have naturally occurring activity patterns that disrupt LTP (Wu et al, 2002;Colgin et al, 2004)-such patterns would only effectively erase very recently encoded potentiation in the apical dendrites but could erase LTP acquired over considerable periods in the basal dendrites. We propose that these erasure patterns operate as periodic 'sweeps' that eliminate relatively little from the one set of synapses (apical) and a great deal from the other (basal).…”

Transition to Seizure: Ictal Discharge Is Preceded by Exhausted Presynaptic GABA Release in the Hippocampal CA3 Region

“…During the preictal state, an enhanced population excitatory drive is mediated by recurrent EPSPs and spontaneous discharges of the pyramidal cells (Cohen and Miles, 2000). At the same time, interneurons discharge cohesively and rhythmically because of their reciprocal inhibition and gap junctional intercommunication (Wu et al, 2002;Zhang et al, 2004), thereby synchronizing the pyramidal neurons (Cobb et al, 1995). Near the end of the preictal state, GABAergic inputs decrease significantly due to transiently exhausted presynaptic GABA release, giving way to high-frequency ictal discharges that are dependent on glutamate and possibly voltage-gated calcium and/or calcium currents, and are unopposed by GABAergic transmission responses at the transition.…”