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Reliability of synaptic transmission at the synapses of Held in vivo under acoustic stimulation.

Englitz B, Tolnai S, Typlt M, Jost J, Rübsamen R - PLoS ONE (2009)

Bottom Line: Its performance is quantified using simulated voltage recordings and found to exhibit a high level of accuracy.By contrast, at the endbulbs of Held in the AVCN failures were found under spontaneous, excited, and suppressed conditions.In accordance with previous studies, failures occurred most abundantly in the suppressed condition, suggesting a role for inhibition.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Mathematics in the Sciences, Leipzig, Germany.

ABSTRACT

Background: The giant synapses of Held play an important role in high-fidelity auditory processing and provide a model system for synaptic transmission at central synapses. Whether transmission of action potentials can fail at these synapses has been investigated in recent studies. At the endbulbs of Held in the anteroventral cochlear nucleus (AVCN) a consistent picture emerged, whereas at the calyx of Held in the medial nucleus of the trapezoid body (MNTB) results on the reliability of transmission remain inconsistent. In vivo this discrepancy could be due to the difficulty in identifying failures of transmission.

Methods/findings: We introduce a novel method for detecting unreliable transmission in vivo. Based on the temporal relationship between a cells' waveform and other potentials in the recordings, a statistical test is developed that provides a balanced decision between the presence and the absence of failures. Its performance is quantified using simulated voltage recordings and found to exhibit a high level of accuracy. The method was applied to extracellular recordings from the synapses of Held in vivo. At the calyces of Held failures of transmission were found only rarely. By contrast, at the endbulbs of Held in the AVCN failures were found under spontaneous, excited, and suppressed conditions. In accordance with previous studies, failures occurred most abundantly in the suppressed condition, suggesting a role for inhibition.

Conclusions/significance: Under the investigated activity conditions/anesthesia, transmission seems to remain largely unimpeded in the MNTB, whereas in the AVCN the occurrence of failures is related to inhibition and could be the basis/result of computational mechanisms for temporal processing. More generally, our approach provides a formal tool for studying the reliability of transmission with high statistical accuracy under typical in vivo recording conditions.

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IAP results and proportion of iPs for AVCN and MNTB for each recording condition.(A) For spontaneous activity the majority (56%) of the AVCN, but less than 5% of the MNTB recordings contained dependent iPs. (B) In the excitatory response condition the percentage of AVCN Dep recordings decreased to 50%. In the MNTB no Dep recordings were found. (C) In the inhibitory/suppressive response condition the percentage of AVCN Dep recordings increased to 80%, whereas again none of the MNTB recordings was classified as Dep. For AVCN Dep recordings the proportion of iPs with respect to the total number of (presynaptic) events estimates the insecurity of transmission (if iPs correspond to failures of transmission). (D) During spontaneous activity No Dep had a significantly smaller iP proportion than Dep, consistent with failures. (E) In the excitatory condition the iP proportion does not differ significantly between the No Dep and the Dep cases, although they both increase compared to the spontaneous condition. (F) In the inh./sup. condition the distribution of iP proportion for the Dep cases increases significantly compared to both previous conditions, whereas the corresponding distribution for the No Dep cases stays similar to the excitatory condition.
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pone-0007014-g006: IAP results and proportion of iPs for AVCN and MNTB for each recording condition.(A) For spontaneous activity the majority (56%) of the AVCN, but less than 5% of the MNTB recordings contained dependent iPs. (B) In the excitatory response condition the percentage of AVCN Dep recordings decreased to 50%. In the MNTB no Dep recordings were found. (C) In the inhibitory/suppressive response condition the percentage of AVCN Dep recordings increased to 80%, whereas again none of the MNTB recordings was classified as Dep. For AVCN Dep recordings the proportion of iPs with respect to the total number of (presynaptic) events estimates the insecurity of transmission (if iPs correspond to failures of transmission). (D) During spontaneous activity No Dep had a significantly smaller iP proportion than Dep, consistent with failures. (E) In the excitatory condition the iP proportion does not differ significantly between the No Dep and the Dep cases, although they both increase compared to the spontaneous condition. (F) In the inh./sup. condition the distribution of iP proportion for the Dep cases increases significantly compared to both previous conditions, whereas the corresponding distribution for the No Dep cases stays similar to the excitatory condition.

Mentions: Across all recording conditions, dependent iPs were frequently found in the AVCN, but rather rarely in the MNTB. In the case of spontaneous activity, 56% (27/48) of the AVCN recordings yielded a Dep result (Figure 6A). For the MNTB, 5% (3/66) of the recordings were classified as Dep.


Reliability of synaptic transmission at the synapses of Held in vivo under acoustic stimulation.

Englitz B, Tolnai S, Typlt M, Jost J, Rübsamen R - PLoS ONE (2009)

IAP results and proportion of iPs for AVCN and MNTB for each recording condition.(A) For spontaneous activity the majority (56%) of the AVCN, but less than 5% of the MNTB recordings contained dependent iPs. (B) In the excitatory response condition the percentage of AVCN Dep recordings decreased to 50%. In the MNTB no Dep recordings were found. (C) In the inhibitory/suppressive response condition the percentage of AVCN Dep recordings increased to 80%, whereas again none of the MNTB recordings was classified as Dep. For AVCN Dep recordings the proportion of iPs with respect to the total number of (presynaptic) events estimates the insecurity of transmission (if iPs correspond to failures of transmission). (D) During spontaneous activity No Dep had a significantly smaller iP proportion than Dep, consistent with failures. (E) In the excitatory condition the iP proportion does not differ significantly between the No Dep and the Dep cases, although they both increase compared to the spontaneous condition. (F) In the inh./sup. condition the distribution of iP proportion for the Dep cases increases significantly compared to both previous conditions, whereas the corresponding distribution for the No Dep cases stays similar to the excitatory condition.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2749334&req=5

pone-0007014-g006: IAP results and proportion of iPs for AVCN and MNTB for each recording condition.(A) For spontaneous activity the majority (56%) of the AVCN, but less than 5% of the MNTB recordings contained dependent iPs. (B) In the excitatory response condition the percentage of AVCN Dep recordings decreased to 50%. In the MNTB no Dep recordings were found. (C) In the inhibitory/suppressive response condition the percentage of AVCN Dep recordings increased to 80%, whereas again none of the MNTB recordings was classified as Dep. For AVCN Dep recordings the proportion of iPs with respect to the total number of (presynaptic) events estimates the insecurity of transmission (if iPs correspond to failures of transmission). (D) During spontaneous activity No Dep had a significantly smaller iP proportion than Dep, consistent with failures. (E) In the excitatory condition the iP proportion does not differ significantly between the No Dep and the Dep cases, although they both increase compared to the spontaneous condition. (F) In the inh./sup. condition the distribution of iP proportion for the Dep cases increases significantly compared to both previous conditions, whereas the corresponding distribution for the No Dep cases stays similar to the excitatory condition.
Mentions: Across all recording conditions, dependent iPs were frequently found in the AVCN, but rather rarely in the MNTB. In the case of spontaneous activity, 56% (27/48) of the AVCN recordings yielded a Dep result (Figure 6A). For the MNTB, 5% (3/66) of the recordings were classified as Dep.

Bottom Line: Its performance is quantified using simulated voltage recordings and found to exhibit a high level of accuracy.By contrast, at the endbulbs of Held in the AVCN failures were found under spontaneous, excited, and suppressed conditions.In accordance with previous studies, failures occurred most abundantly in the suppressed condition, suggesting a role for inhibition.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Mathematics in the Sciences, Leipzig, Germany.

ABSTRACT

Background: The giant synapses of Held play an important role in high-fidelity auditory processing and provide a model system for synaptic transmission at central synapses. Whether transmission of action potentials can fail at these synapses has been investigated in recent studies. At the endbulbs of Held in the anteroventral cochlear nucleus (AVCN) a consistent picture emerged, whereas at the calyx of Held in the medial nucleus of the trapezoid body (MNTB) results on the reliability of transmission remain inconsistent. In vivo this discrepancy could be due to the difficulty in identifying failures of transmission.

Methods/findings: We introduce a novel method for detecting unreliable transmission in vivo. Based on the temporal relationship between a cells' waveform and other potentials in the recordings, a statistical test is developed that provides a balanced decision between the presence and the absence of failures. Its performance is quantified using simulated voltage recordings and found to exhibit a high level of accuracy. The method was applied to extracellular recordings from the synapses of Held in vivo. At the calyces of Held failures of transmission were found only rarely. By contrast, at the endbulbs of Held in the AVCN failures were found under spontaneous, excited, and suppressed conditions. In accordance with previous studies, failures occurred most abundantly in the suppressed condition, suggesting a role for inhibition.

Conclusions/significance: Under the investigated activity conditions/anesthesia, transmission seems to remain largely unimpeded in the MNTB, whereas in the AVCN the occurrence of failures is related to inhibition and could be the basis/result of computational mechanisms for temporal processing. More generally, our approach provides a formal tool for studying the reliability of transmission with high statistical accuracy under typical in vivo recording conditions.

Show MeSH
Related in: MedlinePlus