Abstract
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 modelling 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 transmission electron microscopy (ssTEM) and Focused Ion Beam - Scanning Electron Microscopy (FIB-SEM) 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 in 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 thalamocortical synapses in areas S2 and S1 is similar, supporting the view that both areas can process in parallel specific somatosensory signal streams.
Significance statement Synaptic circuits established by ventral posteromedial (VPM) and posterior (Po) nuclei axons in the first somatosensory area (S1) of rodents are a key in experimental and modelling studies of interactions between the thalamus and cerebral cortex. In addition, VP and Po axons robustly innervate the second somatosensory area (S2) adjacent to S1, yet the structure of their synaptic circuits there were unknown. We combined selective axon labeling with high-end volumetric electron microscopy to measure and compare functionally relevant structural parameters among VP and Po synapses in area S2. We found that the wiring of thalamocortical synapses in S2 is as diverse and specific as those in area S1, supporting the view that both areas process sensory signal streams in parallel.
Footnotes
The Authors declare no competing financial interest.
Bernd Walkenfort, Dr. Mike Hasenberg (Imaging Center Essen-Electron Microscopy Unit, University Hospital, Essen, Germany) and Dr. Javier Conesa (Centro Nacional de Biotecnología - CSIC, Madrid, Spain) for assistance in FIB-SEM image acquisition; and Ms. Brigitte Marshallsay (Forschungszentrum Jülich GmbH, Germany) for her superb technical help in tissue processing and ssTEM imaging.
Spain’s MICINN-AEI grants PCI2019-111900-2 and PID2020-115780GB-I00) to FC. PJMC was the recipient of a pre-doctoral grant from the Spanish Ministry of Science, Innovation and Universities (ref. FPU19/01159).
↵*Both authors share senior authorship
