All-or-none disconnection of pyramidal inputs onto parvalbumin-positive interneurons gates ocular dominance plasticity

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 118; no. 37
• Main Authors: Severin, Daniel, Hong, Su Z, Roh, Seung-Eon, Huang, Shiyong, Zhou, Jiechao, Bridi, Michelle C D, Hong, Ingie, Murase, Sachiko, Robertson, Sarah, Haberman, Rebecca P, Huganir, Richard L, Gallagher, Michela, Quinlan, Elizabeth M, Worley, Paul, Kirkwood, Alfredo
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 14.09.2021
• Subjects: Animals; Biological Sciences; C-Reactive Protein - metabolism; Circuits; Cortex (somatosensory); Deprivation; Dominance, Ocular; Gates (circuits); Interneurons; Interneurons - cytology; Interneurons - physiology; Mice; Mice, Inbred C57BL; Monocular vision; Nerve Tissue Proteins - metabolism; Neural Inhibition; Neural plasticity; Neuronal Plasticity; Ocular dominance; Parvalbumin; Parvalbumins - metabolism; Pyramidal cells; Pyramidal Cells - cytology; Pyramidal Cells - physiology; Receptors, AMPA - metabolism; Receptors, N-Methyl-D-Aspartate - metabolism; Synaptic strength; Visual cortex; Visual Cortex - physiology; Visual deprivation; Visual pathways; synaptic plasticity; NPTX2; visual cortex; neuropentraxin2; disinhibition
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2105388118

Disinhibition is an obligatory initial step in the remodeling of cortical circuits by sensory experience. Our investigation on disinhibitory mechanisms in the classical model of ocular dominance plasticity uncovered an unexpected form of experience-dependent circuit plasticity. In the layer 2/3 of mouse visual cortex, monocular deprivation triggers a complete, "all-or-none," elimination of connections from pyramidal cells onto nearby parvalbumin-positive interneurons (Pyr→PV). This binary form of circuit plasticity is unique, as it is transient, local, and discrete. It lasts only 1 d, and it does not manifest as widespread changes in synaptic strength; rather, only about half of local connections are lost, and the remaining ones are not affected in strength. Mechanistically, the deprivation-induced loss of Pyr→PV is contingent on a reduction of the protein neuropentraxin2. Functionally, the loss of Pyr→PV is absolutely necessary for ocular dominance plasticity, a canonical model of deprivation-induced model of cortical remodeling. We surmise, therefore, that this all-or-none loss of local Pyr→PV circuitry gates experience-dependent cortical plasticity.