Area-specific synapse structure in branched axons reveals a subcellular level of complexity in thalamocortical networks

Abstract

Thalamocortical Posterior nucleus (Po) axons innervating the somatosensory (S1) and motor (MC) vibrissal cortices are key links in the brain neuronal network that allows rodents to explore the environment whisking with their motile vibrissae. Here, using high-end 3D electron microscopy, we demonstrate massive differences between MC vs. S1 Po synapses in a) bouton and active zone size; b) neurotransmitter vesicle pool size; c) mitochondria distribution near synapses; and d) proportion of non-spinous dendrite contacts. These differences are as large, or bigger, than those between Po and ventroposterior thalamic nucleus synapses in S1. Moreover, using single-axon transfection labeling, we show that the structure of boutons in the MC vs. S1 branches of individual Po axons is different. These structural differences parallel striking, recently-discovered divergences in functional efficacy and plasticity between S1 and MC Po synapses, and overall reveal a new, subcellular level of thalamocortical circuit complexity, unaccounted for in current models.