Synaptic organization of cortico-cortical communication in primates

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 if 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.