Long-term potentiation in Schaffer collateral and commissural systems of the hippocampus: In vitro study in rats pretreated with kainic acid

doi:10.1016/0006-8993(83)90570-X

Brain Research

Volume 272, Issue 2, 8 August 1983, Pages 247-253

https://doi.org/10.1016/0006-8993(83)90570-X Get rights and content

Abstract

Experiments were carried out on hippocampal slices from rats pretreated with a unilateral intraventricular injection of kainic acid. The kainic acid produced a lesion of the CA3 area in the hippocampus ipsilateral to the site of injection. The resulting neuroanatomically modified hippocampal slices allowed the independent study of the Schaffer collateral and commissural afferents that synapse onto CA1 pyramidal cells. The Schaffer collateral and commissural afferents were both found to independently hippocampi.

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Long term potentiation in the hippocampus of rats pretreated with kainic acid

J. Physiol. (Lond.)

(1981)

Cited by (16)

Functional preservation of hippocampal CA1 by low-dose GYKI-52466 preconditioning in a rat model of hypoxic-ischemic brain injury
2015, Brain Research
Citation Excerpt :
In the present study, LTP was completely abolished in the few ipsilateral hippocampal slices that could be recovered from HI animals, and markedly reduced in contralateral slices up to 90 days post-HI, without any apparent change in LTD induction. Again, the most likely explanation for this contralateral LTP deficit probably relates to the loss of commissural fibers from the ipsilateral (stroke) side of the brain (Wheal et al., 1983). As such, marked reductions in net synaptic density would reduce cooperative/associative interactions necessary for strong LTP induction (Bliss and Collingridge, 1993; McNaughton, 2003).
Global ischemia during cardiac surgery, brain surgery and stroke leads to lasting neuropsychological impairments. Previously we showed that low-dose GYKI-52466 preconditioning protects against kainic acid-induced seizures and unilateral hypoxic-ischemic (HI) damage in rats. Here, we evaluated low-dose GYKI-52466 on electrophysiological indices of hippocampal CA1 function after HI. Male Sprague-Dawley rats (26 days old) were administered saline or GYKI-52466 (3 mg/kg, s.c.) 90 min before left common carotid artery occlusion and allowed to recover 2 h prior to placement in a hypoxia chamber (1 h; 8% O₂/92% N₂). On days 14 and 90 post-HI, contralateral and, where possible, ipsilateral hippocampal slices were prepared and population spikes and field excitatory postsynaptic potentials (EPSPs) recorded at 30–32 °C. Slices with population spikes ≥3 mV and/or field EPSPs ≥1 mV were accepted for long-term potentiation (LTP) and depression (LTD) studies. GYKI-52466 preconditioning prevented the stroke-induced suppression of population spikes and field EPSPs in both contralateral and ipsilateral hippocampi at 14 and 90 days. On days 14 and 90, both LTP and LTD were readily induced in both contralateral and ipsilateral hippocampi from sham-operated controls. After stroke, LTP was significantly impaired in contralateral and completely absent in ipsilateral hippocampi. In ischemic animals preconditioned with low-dose GYKI-52466, LTP was readily induced on both sides. Hippocampal LTD was unaffected by either HI or GYKI preconditioning on both days 14 and 90. The present results indicate that prophylactic low-dose GYKI-52466 preserves CA1 function and synaptic plasticity processes contralateral, and more importantly, ipsilateral to the site of damage.
Inhibition of hippocampal LTP by ginkgolide B is mediated by its blocking action on PAF rather than glycine receptors
2004, Neurochemistry International
Platelet-activating factor (PAF), a biologically active lipid (1-O-alkyl-2-acetyl-sn-glycero-3-phosphoholine), is identified in different regions of brain, including hippocampus. Specific PAF-activated receptors (PAFRs) are expressed in corresponding brain areas. PAF has been proposed to be a retrograde messenger of long-term potentiation (LTP): the antagonist of PAFRs, ginkgolide B (or BN52021) prevents induction of LTP. Recently it has been found that ginkgolide B is also an efficient blocker of the glycine receptor (GlyR) operated chloride channels (IC₅₀=270±10 nM in hippocampal pyramidal neurons). The question is as follows: is the alteration of LTP by BN52021 due to the PAF antagonism or to the inhibition of glycine-gated chloride channels? We have studied the effects of ginkgolides B and J on LTP induced in the CA1 area of rat hippocampus. Ginkgolide J which is the weakest blocker of PAFR (IC₅₀=54 μM, as compared to IC₅₀=2.5 μM for ginkgolide B) inhibits GlyR-operated channels with IC₅₀=2.0 μM. This assures a convenient concentration window which allows to inhibit GlyR-operated channels without affecting PAFRs. An amount of 5 μM of ginkgolide J did not prevent the induction of LTP, while ginkgolide B (5 μM) completely inhibited this phenomenon. The effect of ginkgolide B on LTP did not alter considerably if GlyRs were blocked by strychnine (2 μM). Strychnine itself had no significant effect on the induction of LTP. Both ginkgolides and strychnine significantly facilitated short-term potentiation (STP). Our data support a hypothesis according to which ginkgolides affect LTP by inhibiting PAFRs.
An efficient method for studying short-term plasticity with random impulse train stimuli
2002, Journal of Neuroscience Methods
In this article, we introduce an efficient method that models quantitatively nonlinear dynamics associated with short-term plasticity (STP) in biological neural systems. It is based on the Voterra–Wiener modeling approach adapted for special stimulus/response datasets. The stimuli are random impulse trains (RITs) of fixed amplitude and Poisson distributed, variable interimpulse intervals. The class of stimuli, we use can be viewed as a hybrid between the paired impulse approach (variable interimpulse interval between two input impulses) and the fixed frequency approach (impulses repeated at fixed intervals, varying in frequency from one stimulus dataset to the next). The responses are sequences of population spike amplitudes of variable size and are assumed to be contemporaneous with the corresponding impulses in the RITs they are evoked by. The nonlinear dynamics of the mechanisms underlying STP are captured by kernels used to create compact STP models with predictive capabilities. Compared to similar methods in the literature, the method presented in this article provides a comprehensive model of STP with considerable improvement in prediction accuracy and requires shorter experimental data collection time.
Molecular mechanisms that underlie structural and functional changes at the postsynaptic membrane during synaptic plasticity
1998, Progress in Neurobiology
The synaptic plasticity that is addressed in this review follows neurodegeneration in the brain and thus has both structural as well as functional components. The model of neurodegeneration that has been selected is the kainic acid lesioned hippocampus. Degeneration of the CA3 pyramidal cells results in a loss of the Schaffer collateral afferents innervating the CA1 pyramidal cells. This is followed by a period of structural plasticity where new synapses are formed. These are associated with changes in the numbers and shapes of spines as well as changes in the morphometry of the dendrites. It is suggested that this synaptogenesis is responsible for an increase in the ratio of NMDA to AMPA receptors mediating excitatory synaptic transmission at these synapses. Changes in the temporal and spatial properties of these synapses resulted in an altered balance between LTP and LTD. These properties together with a reduction in the inhibitory drive increased the excitability of the surviving CA1 pyramidal cells which in turn triggered epileptiform bursting activity. In this review we discuss the insights that may be gained from studies of the underlying molecular machinery.
Developments in one of the collections of the cogs in this machinery has been summarized through recent studies characterizing the roles of neural recognition molecules in synaptic plasticity in the adult nervous systems of vertebrates and invertebrates. Such investigations of neural cell adhesion molecules, cadherins and amyloid precursor protein have shown the involvement of these molecules on the morphogenetic level of synaptic changes, on the one hand, and signal transduction effects, on the other. Further complex cogs are found in the forms of the low-density lipoprotein receptor (LDL-R) family of genes and their ligands play pivotal roles in the brain development and in regulating the growth and remodelling of neurones. Evidence is discussed for their role in the maintenance of cognitive function as well as Alzheimer's. The molecular mechanisms responsible for the clustering and maintenance of transmitter receptors at postsynaptic sites are the final cogs in the machinery that we have reviewed.
Postsynaptic densities (PSD) from excitatory synapses have yielded many cytoskeletal proteins including actin, spectrin, tubulin, microtubule-associated proteins and calcium/calmodulin-dependent protein kinase II. Isolated PSDs have also been shown to be enriched in AMPA, kainate and NMDA receptors. However, recently, a new family of proteins, the MAGUKs (for membrane-associated guanylate kinase) has emerged. The role of these proteins in clustering different NMDA receptor subunits is discussed. The MAGUK proteins are also thought to play a role in synaptic plasticity mediated by nitric oxide (NO). Both NMDA and non-NMDA receptors are highly clustered at excitatory postsynaptic sites in cortical and hippocampal neurones but have revealed differences in their choice of molecular components. Both GABA_A and glycine (Gly) receptors mediate synaptic inhibition in the brain and spinal cord. Whilst little is known about how GABA_A receptors are localized in the postsynaptic membrane, considerable progress has been made towards the elucidation of the molecular mechanisms underlying the formation of Gly receptors. It has been shown that the peripheral membrane protein gephyrin plays a pivotal role in the formation of Gly receptor clusters most likely by anchoring the receptor to the subsynaptic cytoskeleton. Evidence for the distribution as well as function of gephyrin and Gly receptors is discussed. Postsynaptic membrane specializations are complex molecular machinery subserving a multitude of functions in the proper communication between neurones. Despite the fact that only a few key players have been identified it will be a fascinating to watch the story as to how they contribute to structural and functional plasticity unfold.
Plasticity of AMPA and NMDA receptor-mediated epileptiform activity in a chronic model of temporal lobe epilepsy
1995, Epilepsy Research
We have investigated the consequences of tetanic stimulation on epileptiform activity mediated by NMDA and AMPA receptors in an experimental model of human temporal lobe epilepsy. Recordings were performed in the CA1 area of the hippocampus one week following intracerebroventricular injection of kainic acid. Data presented here show that, after tetanic stimulation, there was a long-term increase in the amplitude of the population spikes associated with the epileptiform burst. This activity was triggered by the simultaneous activation of both NMDA and AMPA receptors. However, whilst the pharmacologically isolated AMPA component of this burst underwent long-term enhancement, the NMDA component underwent a long-term decrease in amplitude. These data suggest that in this chronic model of epileptiform activity, there is long-term potentiation of excitatory mediated events regulated primarily by AMPA receptors. Furthermore, the slow time course of the NMDA receptor-mediated synaptic conductances was responsible for prolonging the duration of the epileptiform bursts. However, the powerful depression of NMDA receptor-mediated events following tetanic stimulation suppressed the normally large potentiation of the overall response. Thus although it has been suggested that the NMDA receptor-mediated synaptic events contribute to the epileptogenic properties of the neocortex and hippocampus, this evoked depression may act as an intrinsic anticonvulsant mechanism.
Function of synapses in the CA1 region of the hippocampus: Their contribution to the generation or control of epileptiform activity
1989, Comparative Biochemistry and Physiology -- Part A: Physiology
- 1.
  1. In the kainic acid lesioned hippocampus there is a loss of functional inhibition that is associated with reduction of the IPSPs recorded intracellularly from the surviving CA1 pyramidal cells. The possible pre- or postsynaptic origin of this change has been investigated.
- 2.
  2. Iontophoretic application of GABA to the soma and dendrites of CA1 pyramidal cells indicated that there had been no change in the efficacy of the postsynaptic GABA receptors on these cells.
- 3.
  3. Although a pre-synaptic mechanism is implicated, at one week post lesion we were unable to find any difference in the Ca⁺ dependent K⁺ evoked release of endogenous GABA. However, at survival times greater than 1 week immunohistological studies showed a decrease in the number of somatostatin positive non-pyramidal cells in the stratum oriens of the CA1 area.
- 4.
  4. In addition to the reduction of functional inhibition, changes in excitatory neurotransmitter mechanisms were also found to contribute to the epileptiform burst discharge. A slow component of the epileptiform EPSP recorded from CA1 pyramidal cells has been recorded and was found to be antagonized by the NMDA-receptor antagonist D-APV.
- 5.
  5. Methods of controlling epileptiform activity in the kainic acid lesioned hippocampus have been tested. Stimulation of the substantia nigra and ventral tegmental areas produced profound inhibition of pyramidal cell activity in control hippocampi; however, they were found to be ineffective in controlling the epileptiform burst.
- 6.
  6. A second method involved the use of hippocampal suspension grafts. Whilst this approach has yielded some encouraging data, further studies are necessary before the mechanism of the improvement in inhibitory synaptic function can be explained.

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Long-term potentiation in Schaffer collateral and commissural systems of the hippocampus: In vitro study in rats pretreated with kainic acid

Abstract

Brain Research

Brain Research

Brain Research

Brain Research

Brain Research

Lamellar organisation of hippocampal excitatory pathways

Exp. Brain Res.

A comparison of distal and proximal dendritic synapses on CA1 pyramidals in guinea-pig hippocampal slices in vitro

J. Physiol. (Lond.)

Specific long-lasting potentiation of synaptic transmission in hippocampal slices

Nature (Lond.)

Long lasting potentiation of synaptic transmission in the dentate area of anaesthetised rabbit following perforant path stimulation

J. Physiol. (Lond.)

Dentate area of the unanaesthetised rabbit following stimulation of the perforant path

J. Physiol. (Lond.)

Long term potentiation in the hippocampus of rats pretreated with kainic acid

J. Physiol. (Lond.)