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 Sätzler, Guanxiao Qi, Max Anstotz, Dirk Feldmeyer, Joachim H.R. Lübke*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)3185-3209
Number of pages25
JournalBrain Structure and Function
Volume220
Issue number6
DOIs
StatePublished - Nov 26 2015

Keywords

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

ASJC Scopus subject areas

  • Anatomy
  • Neuroscience(all)
  • Histology

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