Kv3.1 channels regulate the rate of critical period plasticity. (June 2021)

• Record Type: Journal Article
• Authors: Matsuda, Yoshi-Taka; Miyamoto, Hiroyuki; Joho, Rolf H.; Hensch, Takao K
• Is Part Of: Neuroscience research. Volume 167(2021)
• Page Start: 3
• Page End: 10
• Publication Date: 2021-06
• Subjects: MD monocular deprivation -- GABA γ-amino butyric acid -- GAD65 glutamic acid decarboxylase 65 kDa isoform -- PV parvalbumin -- fAHP fast after-hyperpolarization -- EGFP enhanced green fluorescent protein -- DZ diazepam -- WT wild type -- KO knock-out; GABA -- Parvalbumin -- Potassium -- Visual cortex -- Ocular dominance -- Slow-wave sleep -- Benzodiazepine; Neurosciences -- Research -- Periodicals; Neurosciences -- Research -- Japan -- Periodicals; Neurology -- Periodicals; Neurosciences -- Periodicals; Neurosciences -- Recherche -- Périodiques; Neurosciences -- Recherche -- Japon -- Périodiques; Neurosciences -- Research; Japan; Periodicals; 612.8
• DOI: 10.1016/j.neures.2021.04.003
• Languages: English
• ISSNs: 0168-0102

Abstract

Highlights: Kv3.1 potassium channels regulate cortical fast-spiking behavior postnatally. Visual cortical receptive field properties develop normally in the absence of Kv3.1. Sensory plasticity is slowed but critical period timing is normal without Kv3.1. Rate of plasticity reflects Kv3.1 gene dosage controlling prolonged spiking. Diazepam effectively rescues Kv3.1 deficiency of relevance to mental disorders. Abstract: Experience-dependent plasticity within visual cortex is controlled by postnatal maturation of inhibitory circuits, which are both morphologically diverse and precisely connected. Gene-targeted disruption of the voltage-dependent potassium channel Kv 3.1 broadens action potentials and reduces net inhibitory function of parvalbumin (PV)-positive GABA subtypes within the neocortex. In mice lacking Kv 3.1, the rate of input loss from an eye deprived of vision was slowed two-fold, despite otherwise normal critical period timecourse and receptive field properties. Rapid ocular dominance plasticity was restored by local or systemic enhancement of GABAergic transmission with acute benzodiazepine infusion. Diazepam instead exacerbated a global suppression of slow-wave oscillations during sleep described previously in these mutant mice, which therefore did not account for the rescued plasticity. Rapid ocular dominance shifts closely reflected Kv 3.1 gene dosage that prevented prolonged spike discharge of their target pyramidal cells in vivo or the spike amplitude decrement of fast-spiking cells during bouts of high-frequency firing in vitro . Late postnatal expression of this unique channel in fast-spiking interneurons thus subtly regulates the speed of critical period plasticity with implications for mental illnesses.