Pathway-Specific Ultrastructure of Thalamocortical Synapses in Mouse Somatosensory Area S2

The synaptic circuits established by thalamocortical axons from the ventral posteromedial (VPM) and posterior (Po) nuclei in the first somatosensory cortex have been mapped in high detail as they are a prime model in functional and modeling studies of the interactions between the thalamus and cerebral cortex. In addition, VPM and Po neurons innervate the second somatosensory area (S2), but the synaptic organization of their axons in this area remained essentially unknown. On adult male mice, we combined axon labeling with serial section transmission electron microscopy and focused ion beam-scanning electron microscopy to measure and compare functionally relevant structural parameters of synaptic boutons (SBs), e.g., bouton and mitochondrial volume, vesicle pool size, as well as postsynaptic density (PSD) distribution and size. We report that SBs established by caudal VPM and rostral Po synapses resemble each other in their pre- and postsynaptic ultrastructure, while caudal Po SBs are on average 50% smaller in size, number of synaptic vesicles, and total PSD area. We observed a high prevalence (>20%) of small synaptic contacts located in axon intervaricose regions that selectively contact thin, headless dendritic spines (a morphology associated with functionally "silent" synapses). In addition, comparison of the S2 SBs with our previous quantitative data on VPM and Po S1 SBs reveals that the wiring of thalamocortical synapses in Areas S2 and S1 is similar, supporting the view that both areas can process in parallel specific somatosensory signal streams.