TEA-induced long-term potentiation at hippocampal mossy fiber-CA3 synapses: Characteristics of its induction and expression

Suzuki, Etsuko; Okada, Takashi

doi:10.1016/j.brainres.2008.09.101

Cited by 20 publications

(21 citation statements)

References 34 publications

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“…Following washout, we recorded from CA3 pyramidal cells using the patch-clamp technique in the whole-cell mode. As shown previously (Suzuki and Okada, 2009; Zhao et al, 2012), there was a strong potentiation of excitatory postsynaptic potentials (EPSPs) 10–15 min after washout. Next, slice cultures exposed to TEA for 10 min were subjected to HPF and embedded for EM (Zhao et al, 2012).…”

Section: Structural Changes Associated With Functional Plasticity At supporting

confidence: 72%

Structural plasticity of spines at giant mossy fiber synapses

Zhao¹,

Studer²,

Chai³

et al. 2012

Front. Neural Circuits

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The granule cells of the dentate gyrus give rise to thin unmyelinated axons, the mossy fibers. They form giant presynaptic boutons impinging on large complex spines on the proximal dendritic portions of hilar mossy cells and CA3 pyramidal neurons. While these anatomical characteristics have been known for some time, it remained unclear whether functional changes at mossy fiber synapses such as long-term potentiation (LTP) are associated with structural changes. Since subtle structural changes may escape a fine-structural analysis when the tissue is fixed by using aldehydes and is dehydrated in ethanol, rapid high-pressure freezing (HPF) of the tissue was applied. Slice cultures of hippocampus were prepared and incubated in vitro for 2 weeks. Then, chemical LTP (cLTP) was induced by the application of 25 mM tetraethylammonium (TEA) for 10 min. Whole-cell patch-clamp recordings from CA3 pyramidal neurons revealed a highly significant potentiation of mossy fiber synapses when compared to control conditions before the application of TEA. Next, the slice cultures were subjected to HPF, cryosubstitution, and embedding in Epon for a fine-structural analysis. When compared to control tissue, we noticed a significant decrease of synaptic vesicles in mossy fiber boutons and a concomitant increase in the length of the presynaptic membrane. On the postsynaptic side, we observed the formation of small, finger-like protrusions, emanating from the large complex spines. These short protrusions gave rise to active zones that were shorter than those normally found on the thorny excrescences. However, the total number of active zones was significantly increased. Of note, none of these cLTP-induced structural changes was observed in slice cultures from Munc13-1 deficient mouse mutants showing severely impaired vesicle priming and docking. In conclusion, application of HPF allowed us to monitor cLTP-induced structural reorganization of mossy fiber synapses.

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Section: Structural Changes Associated With Functional Plasticity At supporting

confidence: 72%

Structural plasticity of spines at giant mossy fiber synapses

Zhao¹,

Studer²,

Chai³

et al. 2012

Front. Neural Circuits

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“…Based on the assumption that chemical LTP affects virtually all potentiatable synapses in the cultures, in contrast to activation of an indeterminate number of presynaptic fibers by electrical stimulation (Hosokawa et al,1995), we induced LTP by brief (10 minutes) exposure of the slices to 25 mM TEA. Previous electrophysiological studies using a similar protocol have shown that robust LTP is induced under these conditions (Suzuki and Okada,2008). Indeed, when we recorded from CA3 pyramidal neurons, first under control conditions and then after 10 minutes exposure to TEA, we observed strong potentiation of EPSPs (Fig.…”

Section: Resultsmentioning

confidence: 77%

“…For the induction of cLTP, slice cultures were exposed to 25 mM TEA (Sigma, Taufkirchen, Germany) for 10 minutes immediately prior to HPF. This protocol has been shown previously to induce robust cLTP (Suzuki and Okada, 2008). We used this form of LTP because other protocols such as electrical stimulation affect an indeterminate subset of synapses (Hosokawa et al, 1995).…”

Section: Induction Of Chemical Ltpmentioning

confidence: 99%

Structural plasticity of hippocampal mossy fiber synapses as revealed by high‐pressure freezing

Zhao

Studer

Chai

et al. 2012

J of Comparative Neurology

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Despite recent progress in fluorescence microscopy techniques, electron microscopy (EM) is still superior in the simultaneous analysis of all tissue components at high resolution. However, it is unclear to what extent conventional fixation for EM using aldehydes results in tissue alteration. Here we made an attempt to minimize tissue alteration by using rapid high-pressure freezing (HPF) of hippocampal slice cultures. We used this approach to monitor fine-structural changes at hippocampal mossy fiber synapses associated with chemically induced long-term potentiation (LTP). Synaptic plasticity in LTP has been known to involve structural changes at synapses including reorganization of the actin cytoskeleton and de novo formation of spines. While LTP-induced formation and growth of postsynaptic spines have been reported, little is known about associated structural changes in presynaptic boutons. Mossy fiber synapses are assumed to exhibit presynaptic LTP expression and are easily identified by EM. In slice cultures from wildtype mice, we found that chemical LTP increased the length of the presynaptic membrane of mossy fiber boutons, associated with a de novo formation of small spines and an increase in the number of active zones. Of note, these changes were not observed in slice cultures from Munc13-1 knockout mutants exhibiting defective vesicle priming. These findings show that activation of hippocampal mossy fibers induces pre- and postsynaptic structural changes at mossy fiber synapses that can be monitored by EM.

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“…To test this hypothesis, we subjected rats to carotid artery exposure, a necessary procedure for carotid endarterectomy in human. We used tetraethylammonium (TEA), which can induce long term potentiation [17,18], to cause GluR1 trafficking in the hippocampal slices. In addition, we tested the effects of lidocaine, a local anesthetic with anti-inflammatory properties [19], on the cognition and cytokine production after the surgery because lidocaine is effective in attenuating the cognitive dysfunction and cytokine production after isoflurane anesthesia [6,19].…”

Section: Introductionmentioning

confidence: 99%

Critical role of inflammatory cytokines in impairing biochemical processes for learning and memory after surgery in rats

Tan

Cao

Zhang

et al. 2014

J Neuroinflammation

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BackgroundPatients with postoperative cognitive dysfunction have poor outcomes. Neuroinflammation may be the underlying pathophysiology for this dysfunction. We determined whether proinflammatory cytokines affect the trafficking of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors to the plasma membrane, a fundamental biochemical process for learning and memory.MethodsFour-month-old male Fischer 344 rats were subjected to right carotid exposure under isoflurane anesthesia. Some rats received intravenous lidocaine infusion during anesthesia. Rats were tested two weeks later by Barnes maze. The hippocampus was harvested six hours after the surgery for western blotting of interleukin (IL)-1β or IL-6. Hippocampal slices were prepared from control rats or rats subjected to surgery two weeks previously. They were incubated with tetraethylammonium, an agent that can induce long term potentiation, for determining the trafficking of GluR1, an α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor subunit.ResultsSurgery or anesthesia increased the time to identify the target box during the Barnes maze test training sessions and one day after the training sessions. Surgery also prolonged the time to identify the target box eight days after the training sessions. Surgery increased IL-1β and IL-6 in the hippocampus. The tetraethylammonium–induced GluR1 phosphorylation and trafficking were abolished in the hippocampal slices of rats after surgery. These surgical effects were partly inhibited by lidocaine. The incubation of control hippocampal slices with IL-1β and IL-6 abolished tetraethylammonium–induced GluR1 trafficking and phosphorylation. Lidocaine minimally affected the effects of IL-1β on GluR1 trafficking.ConclusionsOur results suggest that surgery increases proinflammatory cytokines that then inhibit GluR1 trafficking, leading to learning and memory impairment.

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TEA-induced long-term potentiation at hippocampal mossy fiber-CA3 synapses: Characteristics of its induction and expression

Cited by 20 publications

References 34 publications

Structural plasticity of spines at giant mossy fiber synapses

Structural plasticity of spines at giant mossy fiber synapses

Structural plasticity of hippocampal mossy fiber synapses as revealed by high‐pressure freezing

Critical role of inflammatory cytokines in impairing biochemical processes for learning and memory after surgery in rats

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