Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body.

Kurt Saetzler, Leander F Söhl, Johann H Bollmann, J. Gerard G Borst, Michael Frotscher, Bert Sakmann, Joachim H R Lübke

    Research output: Contribution to journalArticle

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    Abstract

    The three-dimensional morphology of the axosomatic synaptic structures between a calyx of Held and a principal neuron in the medial nucleus of the trapezoid body (MNTB) in the brainstem of young postnatal day 9 rats was reconstructed from serial ultrathin sections. In the apposition zone between the calyx and the principal neuron two types of membrane specializations were identified: synaptic contacts (SCs) with active zones (AZs) and their associated postsynaptic densities (PSDs) constituted approximately 35% (n = 554) of the specializations; the remaining 65% (n = 1010) were puncta adherentia (PA). Synaptic contacts comprised approximately 5% of the apposition area of presynaptic and postsynaptic membranes. A SC had an average area of 0.100 microm(2), and the nearest neighbors were separated, on average, by 0.59 microm. Approximately one-half of the synaptic vesicles in the calyx were clustered within a distance of 200 nm of the AZ membrane area, a cluster consisting of approximately 60 synaptic vesicles (n = 52 SCs). Approximately two synaptic vesicles per SC were "anatomically docked." Comparing the geometry of the synaptic structure with its previously studied functional properties, we find that during a single presynaptic action potential (AP) (1) approximately 35% of the AZs release a transmitter quantum, (2) the number of SCs and anatomically docked vesicles is comparable with the low estimates of the readily releasable pool (RRP) of quanta, and (3) the broad distribution of PSD areas [coefficient of variation (CV) = 0.9] is likely to contribute to the large variability of miniature EPSC peaks. The geometry of the reconstructed synapse suggests that each of the hundreds of SCs is likely to contribute independently to the size and rising phase of the EPSC during a single AP.
    LanguageEnglish
    Pages10567-10579
    JournalJ Neurosci
    Volume22
    Issue number24
    Publication statusPublished - Dec 2002

    Fingerprint

    Synaptic Vesicles
    Post-Synaptic Density
    Neurons
    Action Potentials
    Membranes
    Synapses
    Brain Stem
    Trapezoid Body

    Keywords

    • Animals
    • Brain Stem
    • Cell Size
    • Cochlear Nucleus
    • Excitatory Postsynaptic Potentials
    • Imaging
    • Three-Dimensional
    • Microscopy
    • Electron
    • Neurons
    • Olivary Nucleus
    • Rats
    • Wistar
    • Receptors
    • Glutamate
    • Synapses
    • Synaptic Membranes
    • Synaptic Vesicles

    Cite this

    Saetzler, K., Söhl, L. F., Bollmann, J. H., Borst, J. G., Frotscher, M., Sakmann, B., & Lübke, J. H. R. (2002). Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci, 22(24), 10567-10579.
    Saetzler, Kurt ; Söhl, Leander F ; Bollmann, Johann H ; Borst, J. Gerard G ; Frotscher, Michael ; Sakmann, Bert ; Lübke, Joachim H R. / Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. In: J Neurosci. 2002 ; Vol. 22, No. 24. pp. 10567-10579.
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    abstract = "The three-dimensional morphology of the axosomatic synaptic structures between a calyx of Held and a principal neuron in the medial nucleus of the trapezoid body (MNTB) in the brainstem of young postnatal day 9 rats was reconstructed from serial ultrathin sections. In the apposition zone between the calyx and the principal neuron two types of membrane specializations were identified: synaptic contacts (SCs) with active zones (AZs) and their associated postsynaptic densities (PSDs) constituted approximately 35{\%} (n = 554) of the specializations; the remaining 65{\%} (n = 1010) were puncta adherentia (PA). Synaptic contacts comprised approximately 5{\%} of the apposition area of presynaptic and postsynaptic membranes. A SC had an average area of 0.100 microm(2), and the nearest neighbors were separated, on average, by 0.59 microm. Approximately one-half of the synaptic vesicles in the calyx were clustered within a distance of 200 nm of the AZ membrane area, a cluster consisting of approximately 60 synaptic vesicles (n = 52 SCs). Approximately two synaptic vesicles per SC were {"}anatomically docked.{"} Comparing the geometry of the synaptic structure with its previously studied functional properties, we find that during a single presynaptic action potential (AP) (1) approximately 35{\%} of the AZs release a transmitter quantum, (2) the number of SCs and anatomically docked vesicles is comparable with the low estimates of the readily releasable pool (RRP) of quanta, and (3) the broad distribution of PSD areas [coefficient of variation (CV) = 0.9] is likely to contribute to the large variability of miniature EPSC peaks. The geometry of the reconstructed synapse suggests that each of the hundreds of SCs is likely to contribute independently to the size and rising phase of the EPSC during a single AP.",
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    author = "Kurt Saetzler and S{\"o}hl, {Leander F} and Bollmann, {Johann H} and Borst, {J. Gerard G} and Michael Frotscher and Bert Sakmann and L{\"u}bke, {Joachim H R}",
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    Saetzler, K, Söhl, LF, Bollmann, JH, Borst, JG, Frotscher, M, Sakmann, B & Lübke, JHR 2002, 'Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body.', J Neurosci, vol. 22, no. 24, pp. 10567-10579.

    Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. / Saetzler, Kurt; Söhl, Leander F; Bollmann, Johann H; Borst, J. Gerard G; Frotscher, Michael; Sakmann, Bert; Lübke, Joachim H R.

    In: J Neurosci, Vol. 22, No. 24, 12.2002, p. 10567-10579.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body.

    AU - Saetzler, Kurt

    AU - Söhl, Leander F

    AU - Bollmann, Johann H

    AU - Borst, J. Gerard G

    AU - Frotscher, Michael

    AU - Sakmann, Bert

    AU - Lübke, Joachim H R

    PY - 2002/12

    Y1 - 2002/12

    N2 - The three-dimensional morphology of the axosomatic synaptic structures between a calyx of Held and a principal neuron in the medial nucleus of the trapezoid body (MNTB) in the brainstem of young postnatal day 9 rats was reconstructed from serial ultrathin sections. In the apposition zone between the calyx and the principal neuron two types of membrane specializations were identified: synaptic contacts (SCs) with active zones (AZs) and their associated postsynaptic densities (PSDs) constituted approximately 35% (n = 554) of the specializations; the remaining 65% (n = 1010) were puncta adherentia (PA). Synaptic contacts comprised approximately 5% of the apposition area of presynaptic and postsynaptic membranes. A SC had an average area of 0.100 microm(2), and the nearest neighbors were separated, on average, by 0.59 microm. Approximately one-half of the synaptic vesicles in the calyx were clustered within a distance of 200 nm of the AZ membrane area, a cluster consisting of approximately 60 synaptic vesicles (n = 52 SCs). Approximately two synaptic vesicles per SC were "anatomically docked." Comparing the geometry of the synaptic structure with its previously studied functional properties, we find that during a single presynaptic action potential (AP) (1) approximately 35% of the AZs release a transmitter quantum, (2) the number of SCs and anatomically docked vesicles is comparable with the low estimates of the readily releasable pool (RRP) of quanta, and (3) the broad distribution of PSD areas [coefficient of variation (CV) = 0.9] is likely to contribute to the large variability of miniature EPSC peaks. The geometry of the reconstructed synapse suggests that each of the hundreds of SCs is likely to contribute independently to the size and rising phase of the EPSC during a single AP.

    AB - The three-dimensional morphology of the axosomatic synaptic structures between a calyx of Held and a principal neuron in the medial nucleus of the trapezoid body (MNTB) in the brainstem of young postnatal day 9 rats was reconstructed from serial ultrathin sections. In the apposition zone between the calyx and the principal neuron two types of membrane specializations were identified: synaptic contacts (SCs) with active zones (AZs) and their associated postsynaptic densities (PSDs) constituted approximately 35% (n = 554) of the specializations; the remaining 65% (n = 1010) were puncta adherentia (PA). Synaptic contacts comprised approximately 5% of the apposition area of presynaptic and postsynaptic membranes. A SC had an average area of 0.100 microm(2), and the nearest neighbors were separated, on average, by 0.59 microm. Approximately one-half of the synaptic vesicles in the calyx were clustered within a distance of 200 nm of the AZ membrane area, a cluster consisting of approximately 60 synaptic vesicles (n = 52 SCs). Approximately two synaptic vesicles per SC were "anatomically docked." Comparing the geometry of the synaptic structure with its previously studied functional properties, we find that during a single presynaptic action potential (AP) (1) approximately 35% of the AZs release a transmitter quantum, (2) the number of SCs and anatomically docked vesicles is comparable with the low estimates of the readily releasable pool (RRP) of quanta, and (3) the broad distribution of PSD areas [coefficient of variation (CV) = 0.9] is likely to contribute to the large variability of miniature EPSC peaks. The geometry of the reconstructed synapse suggests that each of the hundreds of SCs is likely to contribute independently to the size and rising phase of the EPSC during a single AP.

    KW - Animals

    KW - Brain Stem

    KW - Cell Size

    KW - Cochlear Nucleus

    KW - Excitatory Postsynaptic Potentials

    KW - Imaging

    KW - Three-Dimensional

    KW - Microscopy

    KW - Electron

    KW - Neurons

    KW - Olivary Nucleus

    KW - Rats

    KW - Wistar

    KW - Receptors

    KW - Glutamate

    KW - Synapses

    KW - Synaptic Membranes

    KW - Synaptic Vesicles

    M3 - Article

    VL - 22

    SP - 10567

    EP - 10579

    JO - Journal of Neuroscience

    T2 - Journal of Neuroscience

    JF - Journal of Neuroscience

    SN - 1529-2401

    IS - 24

    ER -

    Saetzler K, Söhl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B et al. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci. 2002 Dec;22(24):10567-10579.