Ultrastructural sublaminar-specific diversity of excitatory synaptic boutons in layer 1 of the adult human temporal lobe neocortex.

Abstract

Layer (L)1, beside receiving massive cortico-cortical, commissural and associational projections, is the termination zone of tufted dendrites of pyramidal neurons and the area of Ca²⁺ spike initiation. However, its synaptic organization in humans is not known. Quantitative 3D models of excitatory synaptic boutons (SBs) in L1 of the human temporal lobe neocortex were generated from neocortical biopsy tissue using transmission electron microscopy, 3D-volume reconstructions, and TEM tomography. Particularly, the size of active zones (AZs) and the readily releasable, recycling, and resting pool of synaptic vesicles (SVs) were quantified. The majority of excitatory SBs contained numerous mitochondria comprising ~7% of the total volume, had a large macular, non-perforated AZ (~0.20 µm²) and were predominantly located on dendritic spines. Excitatory SBs had a total pool of ~3500 SVs, a relatively large readily releasable (~4 SVs), recycling (~470 SVs) and resting (~2900 SVs) pool. Astrocytic coverage of excitatory SBs suggests both synaptic crosstalk or removal of spilled glutamate by astrocytic processes at synaptic complexes. The structural composition of SBs in L1 may underlie the function of L1 networks that mediate, integrate, and synchronize contextual and cross-modal information, enabling flexible and state-dependent processing of feedforward sensory inputs from other layers of the cortical column.