Synaptic organization of cortico‐cortical communication in primates

• Published in: The European journal of neuroscience 2020-11, Vol.52 (9), p.4037-4056
• Main Authors: Ashaber, Maria, Zalányi, László, Pálfi, Emese, Stuber, István, Kovács, Tamás, Roe, Anna W., Friedman, Rob M., Négyessy, László
• Format: Article
• Language: English
• Subjects: Animals; axon terminal; Cerebral Cortex; Communication; Cortex (somatosensory); Electron microscopy; human; Light microscopy; Macaca; Microscopy; Microscopy, Electron; Mitochondria; multivariate analyses; Postsynaptic density; Presynapse; Principal components analysis; Saimiri sciureus; serial section reconstruction; Synapses; Synaptogenesis; tract tracing; Visual cortex
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.14905

In cortical circuitry, synaptic communication across areas is based on two types of axon terminals, small and large, with modulatory and driving roles, respectively. In contrast, it is not known whether similar synaptic specializations exist for intra‐areal projections. Using anterograde tracing and three‐dimensional reconstruction by electron microscopy (3D‐EM), we asked whether large boutons form synapses in the circuit of somatosensory cortical areas 3b and 1. In contrast to observations in macaque visual cortex, light microscopy showed both small and large boutons not only in inter‐areal pathways, but also in long‐distance intrinsic connections. 3D‐EM showed that correlation of surface and volume provides a powerful tool for classifying cortical endings. Principal component analysis supported this observation and highlighted the significance of the size of mitochondria as a distinguishing feature of bouton type. The larger mitochondrion and higher degree of perforated postsynaptic density associated with large rather than to small boutons support the driver‐like function of large boutons. In contrast to bouton size and complexity, the size of the postsynaptic density appeared invariant across the bouton types. Comparative studies in human supported that size is a major distinguishing factor of bouton type in the cerebral cortex. In conclusion, the driver‐like function of the large endings could facilitate fast dissemination of tactile information within the intrinsic and inter‐areal circuitry of areas 3b and 1. We report here that cortical axon terminals can be grouped into distinct small and large synaptic bouton types based on their three dimensional ultrastructural properties. Three‐D serial section electron microscopic reconstructions of squirrel monkeys and human boutons revealed that surface and volume were highly correlated and grouped boutons. A multivariate principal component analysis of ultrastructural features further supports this distinction.