Myelination of parvalbumin interneurons shapes the function of cortical sensory inhibitory circuits

Abstract Myelination of projection neurons by oligodendrocytes is key to optimize action potential conduction over long distances. However, a large fraction of myelin enwraps the axons of parvalbumin-positive fast-spiking interneurons (FSI), exclusively involved in local cortical circuits. Whether F...

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Published inNature communications Vol. 11; no. 1; p. 5151
Main Authors Benamer, Najate, Vidal, Marie, Balia, Maddalena, Angulo, María Cecilia
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group 13.10.2020
Nature Publishing Group UK
Nature Portfolio
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Summary:Abstract Myelination of projection neurons by oligodendrocytes is key to optimize action potential conduction over long distances. However, a large fraction of myelin enwraps the axons of parvalbumin-positive fast-spiking interneurons (FSI), exclusively involved in local cortical circuits. Whether FSI myelination contributes to the fine‐tuning of intracortical networks is unknown. Here we demonstrate that FSI myelination is required for the establishment and maintenance of the powerful FSI-mediated feedforward inhibition of cortical sensory circuits. The disruption of GABAergic synaptic signaling of oligodendrocyte precursor cells prior to myelination onset resulted in severe FSI myelination defects characterized by longer internodes and nodes, aberrant myelination of branch points and proximal axon malformation. Consequently, high-frequency FSI discharges as well as FSI-dependent postsynaptic latencies and strengths of excitatory neurons were reduced. These dysfunctions generated a strong excitation-inhibition imbalance that correlated with whisker-dependent texture discrimination impairments. FSI myelination is therefore critical for the function of mature cortical inhibitory circuits.
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ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-020-18984-7