Volume electron microscopy of the distribution of synapses in the neuropil of the juvenile rat somatosensory cortex

Abstract

Knowing the proportions of asymmetric (excitatory) and symmetric (inhibitory) synapses in the neuropil is critical for understanding the design of cortical circuits. We used focused ion beam milling and scanning electron microscopy (FIB/SEM) to obtain stacks of serial sections from the six layers of the juvenile rat (postnatal day 14) somatosensory cortex (hindlimb representation). We segmented in three-dimensions 6184 synaptic junctions and determined whether they were established on dendritic spines or dendritic shafts. Of all these synapses, 87–94% were asymmetric and 6–13% were symmetric. Asymmetric synapses were preferentially located on dendritic spines in all layers (80–91%) while symmetric synapses were mainly located on dendritic shafts (62–86%). Furthermore, we found that less than 6% of the dendritic spines establish more than one synapse. The vast majority of axospinous synapses were established on the spine head. Synapses on the spine neck were scarce, although they were more common when the dendritic spine established multiple synapses. This study provides a new large quantitative dataset that may contribute not only to the knowledge of the ultrastructure of the cortex, but also towards defining the connectivity patterns through all cortical layers.Electronic supplementary materialThe online version of this article (doi:10.1007/s00429-017-1470-7) contains supplementary material, which is available to authorized users.

Three-dimensional synaptic organization of the human hippocampal CA1 field

“…It has also been consistently reported that the neuropil is characterized by a much higher number of excitatory contacts compared to inhibitory synapses in different brain regions and species (4,11,(27)(28)(29)(30). In the present study, the density of inhibitory synapses was particularly low in most CA1 layers (AS:SS ratio in all layers was around 95:5 except for in SLM, where the ratio was close to 90:10).…”

“…Regarding postsynaptic preferences, we observed a clear preference of excitatory axons and inhibitory axons for dendritic spines and dendritic shafts, respectively, which is also characteristic in other cortical regions and species, although variations in their percentages have been reported (4,12,27,28,(30)(31)(32). For example, axospinous AS are especially abundant in sSP (87.61%) when compared to other brain regions in both humans and other species such as layer II of the human transentorhinal cortex, where axospinous AS account for only 55% of the total synaptic population (12).…”

“…While synaptic density differed across layers, the spatial organization of synapses was consistently random in all layers. Randomly distributed synapses have also been described in the somatosensory cortex of rats and the frontal and transentorhinal cortices of the human brain (11,15,26,27), suggesting that this synaptic characteristic is a widespread 'rule' of the cerebral cortex of different species.…”

3d Synaptic Organization of the Rat Ca1 and Alterations Induced by Cocaine Self-Administration

“…It has been consistently reported that the neuropil is characterized by a much higher number of excitatory contacts compared to inhibitory synapses in different brain regions and species 34,35,36,37,38,39,24 . In the present study, we found that the AS:SS ratio was 96.25:3.75.…”

“…However, it has been well established via electron microscopy that dendritic shafts also form synapses and not all dendritic spines represent postsynaptic targets 23,24,25 . Thus, electron microscopy with serial section reconstruction is the gold standard method for studying the normal synaptic organization and its possible alterations.…”