Structural determinants underlying the high efficacy of synaptic transmission and plasticity at synaptic boutons in layer 4 of the adult rat 'barrel cortex'

Astrid Rollenhagen, Kerstin Klook, Kurt Saetzler, Guanxiao Qi, Max Anstötz, Dirk Feldmeyer, Joachim H R Lübke

    Research output: Contribution to journalArticle

    11 Citations (Scopus)

    Abstract

    Excitatory layer 4 (L4) neurons in the 'barrel field' of the rat somatosensory cortex represent an important component in thalamocortical information processing. However, no detailed information exists concerning the quantitative geometry of synaptic boutons terminating on these neurons. Thus, L4 synaptic boutons were investigated using serial ultrathin sections and subsequent quantitative 3D reconstructions. In particular, parameters representing structural correlates of synaptic transmission and plasticity such as the number, size and distribution of pre- and postsynaptic densities forming the active zone (AZ) and of the three functionally defined pools of synaptic vesicles were analyzed. L4 synaptic boutons varied substantially in shape and size; the majority had a single, but large AZ with opposing pre- and postsynaptic densities that matched perfectly in size and position. More than a third of the examined boutons showed perforations of the postsynaptic density. Synaptic boutons contained on average a total pool of 561 ± 108 vesicles, with ~5 \% constituting the putative readily releasable, ~23 \% the recycling, and the remainder the reserve pool. These pools are comparably larger than other characterized central synapses. Synaptic complexes were surrounded by a dense network of fine astrocytic processes that reached as far as the synaptic cleft, thus regulating the temporal and spatial glutamate concentration, and thereby shaping the unitary EPSP amplitude. In summary, the geometry and size of AZs, the comparably large readily releasable and recycling pools, together with the tight astrocytic ensheathment, may explain and contribute to the high release probability, efficacy and modulation of synaptic transmission at excitatory L4 synaptic boutons. Moreover, the structural variability as indicated by the geometry of L4 synaptic boutons, the presence of mitochondria and the size and shape of the AZs strongly suggest that synaptic reliability, strength and plasticity is governed and modulated individually at excitatory L4 synaptic boutons.
    LanguageEnglish
    Pages3185-3209
    JournalBrain Structure and Function
    Volume220
    Issue number6
    DOIs
    Publication statusPublished - Nov 2015

    Fingerprint

    Neuronal Plasticity
    Presynaptic Terminals
    Synaptic Transmission
    Post-Synaptic Density
    Recycling
    Mitochondrial Size
    Neurons
    Somatosensory Cortex
    Synaptic Vesicles
    Excitatory Postsynaptic Potentials
    Automatic Data Processing
    Synapses
    Glutamic Acid

    Keywords

    • Barrel cortex Layer 4 synaptic boutons Quantitative 3D reconstructions Distinct pools of synaptic vesicles Synaptic transmission and plasticity

    Cite this

    Rollenhagen, Astrid ; Klook, Kerstin ; Saetzler, Kurt ; Qi, Guanxiao ; Anstötz, Max ; Feldmeyer, Dirk ; Lübke, Joachim H R. / Structural determinants underlying the high efficacy of synaptic transmission and plasticity at synaptic boutons in layer 4 of the adult rat 'barrel cortex'. In: Brain Structure and Function. 2015 ; Vol. 220, No. 6. pp. 3185-3209.
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    abstract = "Excitatory layer 4 (L4) neurons in the 'barrel field' of the rat somatosensory cortex represent an important component in thalamocortical information processing. However, no detailed information exists concerning the quantitative geometry of synaptic boutons terminating on these neurons. Thus, L4 synaptic boutons were investigated using serial ultrathin sections and subsequent quantitative 3D reconstructions. In particular, parameters representing structural correlates of synaptic transmission and plasticity such as the number, size and distribution of pre- and postsynaptic densities forming the active zone (AZ) and of the three functionally defined pools of synaptic vesicles were analyzed. L4 synaptic boutons varied substantially in shape and size; the majority had a single, but large AZ with opposing pre- and postsynaptic densities that matched perfectly in size and position. More than a third of the examined boutons showed perforations of the postsynaptic density. Synaptic boutons contained on average a total pool of 561 ± 108 vesicles, with ~5 \{\%} constituting the putative readily releasable, ~23 \{\%} the recycling, and the remainder the reserve pool. These pools are comparably larger than other characterized central synapses. Synaptic complexes were surrounded by a dense network of fine astrocytic processes that reached as far as the synaptic cleft, thus regulating the temporal and spatial glutamate concentration, and thereby shaping the unitary EPSP amplitude. In summary, the geometry and size of AZs, the comparably large readily releasable and recycling pools, together with the tight astrocytic ensheathment, may explain and contribute to the high release probability, efficacy and modulation of synaptic transmission at excitatory L4 synaptic boutons. Moreover, the structural variability as indicated by the geometry of L4 synaptic boutons, the presence of mitochondria and the size and shape of the AZs strongly suggest that synaptic reliability, strength and plasticity is governed and modulated individually at excitatory L4 synaptic boutons.",
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    Structural determinants underlying the high efficacy of synaptic transmission and plasticity at synaptic boutons in layer 4 of the adult rat 'barrel cortex'. / Rollenhagen, Astrid; Klook, Kerstin; Saetzler, Kurt; Qi, Guanxiao; Anstötz, Max; Feldmeyer, Dirk; Lübke, Joachim H R.

    In: Brain Structure and Function, Vol. 220, No. 6, 11.2015, p. 3185-3209.

    Research output: Contribution to journalArticle

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    AU - Rollenhagen, Astrid

    AU - Klook, Kerstin

    AU - Saetzler, Kurt

    AU - Qi, Guanxiao

    AU - Anstötz, Max

    AU - Feldmeyer, Dirk

    AU - Lübke, Joachim H R

    PY - 2015/11

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    AB - Excitatory layer 4 (L4) neurons in the 'barrel field' of the rat somatosensory cortex represent an important component in thalamocortical information processing. However, no detailed information exists concerning the quantitative geometry of synaptic boutons terminating on these neurons. Thus, L4 synaptic boutons were investigated using serial ultrathin sections and subsequent quantitative 3D reconstructions. In particular, parameters representing structural correlates of synaptic transmission and plasticity such as the number, size and distribution of pre- and postsynaptic densities forming the active zone (AZ) and of the three functionally defined pools of synaptic vesicles were analyzed. L4 synaptic boutons varied substantially in shape and size; the majority had a single, but large AZ with opposing pre- and postsynaptic densities that matched perfectly in size and position. More than a third of the examined boutons showed perforations of the postsynaptic density. Synaptic boutons contained on average a total pool of 561 ± 108 vesicles, with ~5 \% constituting the putative readily releasable, ~23 \% the recycling, and the remainder the reserve pool. These pools are comparably larger than other characterized central synapses. Synaptic complexes were surrounded by a dense network of fine astrocytic processes that reached as far as the synaptic cleft, thus regulating the temporal and spatial glutamate concentration, and thereby shaping the unitary EPSP amplitude. In summary, the geometry and size of AZs, the comparably large readily releasable and recycling pools, together with the tight astrocytic ensheathment, may explain and contribute to the high release probability, efficacy and modulation of synaptic transmission at excitatory L4 synaptic boutons. Moreover, the structural variability as indicated by the geometry of L4 synaptic boutons, the presence of mitochondria and the size and shape of the AZs strongly suggest that synaptic reliability, strength and plasticity is governed and modulated individually at excitatory L4 synaptic boutons.

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