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J Neurosci. 2020 Feb 11. pii: 2886-19. doi: 10.1523/JNEUROSCI.2886-19.2020. [Epub ahead of print]

Area-specific synapse structure in branched posterior nucleus axons reveals a new level of complexity in thalamocortical networks.

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Department of Anatomy & Neuroscience, School of Medicine, Autónoma de Madrid University, 28029 Madrid, Spain.
Institute of Neuroscience and Medicine INM-10, Research Centre Jülich GmbH, 52425 Jülich, Germany.
Laboratorio Cajal de Circuitos Corticales, Centro de Tecnología Biomédica, Universidad Politécnica de Madrid, Pozuelo de Alarcón, 28223 Madrid, Spain.
CIBERNED, Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas.
Departamento de Arquitectura y Tecnología de Sistemas Informáticos, Universidad Politécnica de Madrid. Boadilla del Monte, 28660, Madrid, Spain.
Instituto Cajal, Consejo Superior de Investigaciones Científicas, Calle Av. Arce 37 28002, Madrid, Spain.
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty RWTH University Hospital Aachen, 52074 Aachen, Germany.
JARA-Translational Brain Medicine, Jülich-Aachen, Germany.
Department of Anatomy & Neuroscience, School of Medicine, Autónoma de Madrid University, 28029 Madrid, Spain


Thalamocortical Posterior nucleus (Po) axons innervating the vibrissal somatosensory (S1) and motor (MC) cortices are key links in the brain neuronal network that allows rodents to explore the environment whisking with their motile snout vibrissae. Here, using fine-scale high-end 3D electron microscopy, we demonstrate in adult male C57BL/6 wildtype mice marked differences between MC vs. S1 Po synapses in a) bouton and active zone size; b) neurotransmitter vesicle pool size; c) distribution of mitochondria around synapses; and d) proportion of synapses established on dendritic spines and dendritic shafts. These differences are as large, or even more pronounced, than those between Po and ventroposterior thalamic nucleus synapses in S1. Moreover, using single-axon transfection labeling, we demonstrate that the above differences actually occur on the MC vs. the S1 branches of individual Po cell axons that innervate both areas. Along with recently-discovered divergences in efficacy and plasticity, the synaptic structure differences reported here thus reveal a new subcellular level of complexity. This is a finding that upends current models of thalamocortical circuitry, and that might as well illuminate the functional logic of other branched projection axon systems.SIGNIFICANCE STATEMENTMany long-distance brain connections depend on neurons whose branched axons target separate regions. Using 3D electron microscopy and single-cell transfection, we investigated the mouse Posterior thalamic nucleus (Po) cell axons that simultaneously innervate motor and sensory areas of the cerebral cortex involved in whisker movement control. We demonstrate significant differences in the size of the boutons made in each area by individual Po axons, as well as in functionally-relevant parameters in the composition of their synapses. In addition, we found similarly large differences between the synapses of Po vs. ventral posteromedial thalamic nucleus axons in the whisker sensory cortex. Area-specific synapse structure in individual axons implies a new, unsuspected level of complexity in long-distance brain connections.

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