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Dendritic spine dynamics in synaptogenesis after repeated LTP inductions: dependence on pre-existing spine density.

Oe Y, Tominaga-Yoshino K, Hasegawa S, Ogura A - Sci Rep (2013)

Bottom Line: Here we examined the dynamics of individual dendritic spines after repeated LTP-inductions and found the existence of two phases in the spines' stochastic behavior that eventually lead to the increase in spine density.This spine dynamics occurred preferentially in the dendritic segments having low pre-existing spine density.Our results may provide clues for understanding the cellular bases underlying the repetition-dependent consolidation of memory.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Osaka University Graduate School of Frontier Biosciences, Suita, Osaka, Japan. oguraa@fbs.osaka-u.ac.jp

ABSTRACT
Not only from our daily experience but from learning experiments in animals, we know that the establishment of long-lasting memory requires repeated practice. However, cellular backgrounds underlying this repetition-dependent consolidation of memory remain largely unclear. We reported previously using organotypic slice cultures of rodent hippocampus that the repeated inductions of LTP (long-term potentiation) lead to a slowly developing long-lasting synaptic enhancement accompanied by synaptogenesis distinct from LTP itself, and proposed this phenomenon as a model system suitable for the analysis of the repetition-dependent consolidation of memory. Here we examined the dynamics of individual dendritic spines after repeated LTP-inductions and found the existence of two phases in the spines' stochastic behavior that eventually lead to the increase in spine density. This spine dynamics occurred preferentially in the dendritic segments having low pre-existing spine density. Our results may provide clues for understanding the cellular bases underlying the repetition-dependent consolidation of memory.

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Increase in spine density after 3 repeated inductions of chemical LTP in cultured mouse hippocampal slices.(a) Timeline of experimental procedures. The day of 3 LTP inductions ( = PS [poststimulus] day 0) typically corresponds to 17 DIV (days in vitro). Images were obtained 4 times at PS days −1, 3, 6 and 10. (b) Chemical inductions of LTP (representative recording). Note that the EPSP amplitude increases without any need of test stimuli. This nature is important, since we delivered no electric pulses for RISE production. (c) Representative time-sequenced images of dendritic segments. Plus and minus symbols in each picture indicate the spines generated and retracted, respectively, as determined by comparing 2 time-consecutive images. (d) Development of RISE after 3 LTP inductions. Note here that 3FK specimens show no net spine density increase at PS day 3. The numbers of dendritic segments examined are 30, 32 and 42, for No stim, 1FK and 3FK specimens, respectively. Statistic comparison was made by 2-way ANOVA followed by Bonferroni's test. P values are 0.038 for *1, 0.0057 for **2 and 0.0098 for **3.
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f1: Increase in spine density after 3 repeated inductions of chemical LTP in cultured mouse hippocampal slices.(a) Timeline of experimental procedures. The day of 3 LTP inductions ( = PS [poststimulus] day 0) typically corresponds to 17 DIV (days in vitro). Images were obtained 4 times at PS days −1, 3, 6 and 10. (b) Chemical inductions of LTP (representative recording). Note that the EPSP amplitude increases without any need of test stimuli. This nature is important, since we delivered no electric pulses for RISE production. (c) Representative time-sequenced images of dendritic segments. Plus and minus symbols in each picture indicate the spines generated and retracted, respectively, as determined by comparing 2 time-consecutive images. (d) Development of RISE after 3 LTP inductions. Note here that 3FK specimens show no net spine density increase at PS day 3. The numbers of dendritic segments examined are 30, 32 and 42, for No stim, 1FK and 3FK specimens, respectively. Statistic comparison was made by 2-way ANOVA followed by Bonferroni's test. P values are 0.038 for *1, 0.0057 for **2 and 0.0098 for **3.

Mentions: Although there are multiple means for producing RISE101114, we chose here the application of forskolin (FK), since there is a report4 that memory consolidation requires repeated PKA activations in vivo. This choice may allow better comparison of the results we obtain here with the previous knowledge. First we confirmed that FK (20 μM, 20 min) induces LTP in the Schaffer collateral-CA1 pyramidal cell synapses in mouse slice cultures as it does in rat slice cultures8 (Fig. 1a, b). Three repeated inductions of LTP at 6 h intervals was effective to produce RISE in mouse cultures as was the case of rat cultures. Moreover, the time-course of development of RISE, including an apparent delay between the third LTP and the onset of synaptic enhancement, was similar to that of rat cultures (Fig. 1c, d). Single induction of LTP (indicated as “1FK”) or repeated medium renewal (indicatd as “No stim”) did not produce RISE-like synaptic enhancement.


Dendritic spine dynamics in synaptogenesis after repeated LTP inductions: dependence on pre-existing spine density.

Oe Y, Tominaga-Yoshino K, Hasegawa S, Ogura A - Sci Rep (2013)

Increase in spine density after 3 repeated inductions of chemical LTP in cultured mouse hippocampal slices.(a) Timeline of experimental procedures. The day of 3 LTP inductions ( = PS [poststimulus] day 0) typically corresponds to 17 DIV (days in vitro). Images were obtained 4 times at PS days −1, 3, 6 and 10. (b) Chemical inductions of LTP (representative recording). Note that the EPSP amplitude increases without any need of test stimuli. This nature is important, since we delivered no electric pulses for RISE production. (c) Representative time-sequenced images of dendritic segments. Plus and minus symbols in each picture indicate the spines generated and retracted, respectively, as determined by comparing 2 time-consecutive images. (d) Development of RISE after 3 LTP inductions. Note here that 3FK specimens show no net spine density increase at PS day 3. The numbers of dendritic segments examined are 30, 32 and 42, for No stim, 1FK and 3FK specimens, respectively. Statistic comparison was made by 2-way ANOVA followed by Bonferroni's test. P values are 0.038 for *1, 0.0057 for **2 and 0.0098 for **3.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3674431&req=5

f1: Increase in spine density after 3 repeated inductions of chemical LTP in cultured mouse hippocampal slices.(a) Timeline of experimental procedures. The day of 3 LTP inductions ( = PS [poststimulus] day 0) typically corresponds to 17 DIV (days in vitro). Images were obtained 4 times at PS days −1, 3, 6 and 10. (b) Chemical inductions of LTP (representative recording). Note that the EPSP amplitude increases without any need of test stimuli. This nature is important, since we delivered no electric pulses for RISE production. (c) Representative time-sequenced images of dendritic segments. Plus and minus symbols in each picture indicate the spines generated and retracted, respectively, as determined by comparing 2 time-consecutive images. (d) Development of RISE after 3 LTP inductions. Note here that 3FK specimens show no net spine density increase at PS day 3. The numbers of dendritic segments examined are 30, 32 and 42, for No stim, 1FK and 3FK specimens, respectively. Statistic comparison was made by 2-way ANOVA followed by Bonferroni's test. P values are 0.038 for *1, 0.0057 for **2 and 0.0098 for **3.
Mentions: Although there are multiple means for producing RISE101114, we chose here the application of forskolin (FK), since there is a report4 that memory consolidation requires repeated PKA activations in vivo. This choice may allow better comparison of the results we obtain here with the previous knowledge. First we confirmed that FK (20 μM, 20 min) induces LTP in the Schaffer collateral-CA1 pyramidal cell synapses in mouse slice cultures as it does in rat slice cultures8 (Fig. 1a, b). Three repeated inductions of LTP at 6 h intervals was effective to produce RISE in mouse cultures as was the case of rat cultures. Moreover, the time-course of development of RISE, including an apparent delay between the third LTP and the onset of synaptic enhancement, was similar to that of rat cultures (Fig. 1c, d). Single induction of LTP (indicated as “1FK”) or repeated medium renewal (indicatd as “No stim”) did not produce RISE-like synaptic enhancement.

Bottom Line: Here we examined the dynamics of individual dendritic spines after repeated LTP-inductions and found the existence of two phases in the spines' stochastic behavior that eventually lead to the increase in spine density.This spine dynamics occurred preferentially in the dendritic segments having low pre-existing spine density.Our results may provide clues for understanding the cellular bases underlying the repetition-dependent consolidation of memory.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Osaka University Graduate School of Frontier Biosciences, Suita, Osaka, Japan. oguraa@fbs.osaka-u.ac.jp

ABSTRACT
Not only from our daily experience but from learning experiments in animals, we know that the establishment of long-lasting memory requires repeated practice. However, cellular backgrounds underlying this repetition-dependent consolidation of memory remain largely unclear. We reported previously using organotypic slice cultures of rodent hippocampus that the repeated inductions of LTP (long-term potentiation) lead to a slowly developing long-lasting synaptic enhancement accompanied by synaptogenesis distinct from LTP itself, and proposed this phenomenon as a model system suitable for the analysis of the repetition-dependent consolidation of memory. Here we examined the dynamics of individual dendritic spines after repeated LTP-inductions and found the existence of two phases in the spines' stochastic behavior that eventually lead to the increase in spine density. This spine dynamics occurred preferentially in the dendritic segments having low pre-existing spine density. Our results may provide clues for understanding the cellular bases underlying the repetition-dependent consolidation of memory.

Show MeSH