Reduction of long-term potentiation at Schaffer collateral-CA1 synapses in the rat hippocampus at the acute stage of vestibular compensation

Abstract

Vestibular compensation is a recovery process from vestibular symptoms over time after unilateral loss of peripheral vestibular end organs. The aim of the present study was to observe time-dependent changes in long-term potentiation (LTP) at Schaffer collateral-CA1 synapses in the CA1 area of the hippocampus during vestibular compensation. The input-output (I/O) relationships of fEPSP amplitudes and LTP induced by theta burst stimulation to Schaffer's collateral commissural fibers were evaluated from the CA1 area of hippocampal slices at 1 day, 1 week, and 1 month after unilateral labyrinthectomy (UL). The I/O relationships of fEPSPs in the CA1 area was significantly reduced within 1 week post-op and then showed a non-significant reduction at 1 month after UL. Compared with sham-operated animals, there was a significant reduction of LTP induction in the hippocampus at 1 day and 1 week after UL. However, LTP induction levels in the CA1 area of the hippocampus also returned to those of sham-operated animals 1 month following UL. These data suggest that unilateral injury of the peripheral vestibular end organs results in a transient deficit in synaptic plasticity in the CA1 hippocampal area at acute stages of vestibular compensation.

Vestibular Modulation of Long-Term Potentiation and NMDA Receptor Expression in the Hippocampus

“…From Truchet et al (2019) with permission. slope or PS amplitude without LTP, that was reported in the in vitro studies (Zheng et al, 2003;Lee et al, 2017), which is very interesting. This suggests that UVL and BVL may have completely different effects on the intrinsic excitability of the neurons in the hippocampus, perhaps due to the asymmetrical effects of UVL on the CNS.…”

“…In both cases, a UVL was performed and then hippocampal slices removed. However, the LTP results of Lee et al (2017) appear inconsistent with those obtained by Zheng et al (2010) FIGURE 4 | Input-output analysis in anesthetized animals, 7 months after surgery. There were no significant differences in fEPSP slope for either CA1 (A) or DG (B), or in DG population spike height (C), between the sham (open circles) and BVD (filled circles) groups.…”

“…In vitro studies of the hippocampus necessarily mean that all remaining vestibular input, as well as that from all other cranial nerves, is removed, so that if the vestibular lesion was a UVL, then the vestibular input from the other ear is removed as well. Lee et al (2017) conducted an in vitro study of the effects of surgical UVL in rats on LTP in CA1 in hippocampal slices. The rationale for this study was to investigate whether unilateral loss of vestibular input would affect LTP induced in the hippocampus, in vitro.…”

“…Nevertheless, three points could partially explain the discrepancies. First, recordings were performed with a 21-23 • C ACSF by Zheng et al (2003) and 30 • C by Lee et al (2017), which can affect the membrane properties of the neurons and thus the evoked potential (Deisz, 1999;Volgushev et al, 2000;Liebregts et al, 2002). Second, the time points were different, with Zheng et al (2003) using 4-6 weeks or 5-6 months following the lesion and Lee et al (2017) using 1 day, 1 week, and 1 month (equivalent to 4-6 weeks) postlesion.…”

“…In terms of the two in vitro studies, what they have in common is that they removed hippocampal slices from rats that had received a UVL, at similar time points, and they recorded field potentials in the slices at various times postlesion. Both Zheng et al (2003) and Lee et al (2017) reported that the fEPSP slope was reduced following UVL, suggesting a decrease in excitability, in vitro, as a result of the lost vestibular input. In both cases, the effect was bilateral, which supports the evidence that vestibular information from one vestibular labyrinth is transmitted to both hippocampi (Cuthbert et al, 2000;Rancz et al, 2015).…”