title: Removal of Perineuronal Nets Unlocks Juvenile Plasticity Through Network Mechanisms of Decreased Inhibition and Increased Gamma Activity.
abstract: Perineuronal nets (PNNs) are extracellular matrix structures mainly enwrapping parvalbumin-expressing inhibitory neurons. The assembly of PNNs coincides with the end of the period of heightened visual cortex plasticity in juveniles, whereas removal of PNNs in adults reopens for plasticity. The mechanisms underlying this phenomenon remain elusive. We have used chronic electrophysiological recordings to investigate accompanying electrophysiological changes to activity-dependent plasticity and we report on novel mechanisms involved in both induced and critical period plasticity. By inducing activity-dependent plasticity in the visual cortex of adult rats while recording single unit and population activity, we demonstrate that PNN removal alters the balance between inhibitory and excitatory spiking activity directly. Without PNNs, inhibitory activity was reduced, whereas spiking variability was increased as predicted in a simulation with a Brunel neural network. Together with a shift in ocular dominance and large effects on unit activity during the first 48 h of monocular deprivation (MD), we show that PNN removal resets the neural network to an immature, juvenile state. Furthermore, in PNN-depleted adults as well as in juveniles, MD caused an immediate potentiation of gamma activity, suggesting a novel mechanism initiating activity-dependent plasticity and driving the rapid changes in unit activity.
  
  
  
  Emerging evidence suggests a role for perineuronal nets (PNNs) in learning and regulation of plasticity, but the underlying mechanisms remain unresolved. Here, we used chronic in vivo extracellular recordings to investigate how removal of PNNs opens for plasticity and how activity-dependent plasticity affects neural activity over time. PNN removal caused reduced inhibitory activity and reset the network to a juvenile state. Experimentally induced activity-dependent plasticity by monocular deprivation caused rapid changes in single unit activity and a remarkable potentiation of gamma oscillations. Our results demonstrate how PNNs may be involved directly in stabilizing the neural network. Moreover, the immediate potentiation of gamma activity after plasticity onset points to potential new mechanisms for the initiation of activity-dependent plasticity.
authors.affiliation: Department of Biosciences.|Center for Integrative Neuroplasticity, University of Oslo, 0370 Oslo, Norway.
authors.forename: Kristian Kinden
authors.identifier: 0000-0003-3145-1659
authors.initials: KK
authors.lastname: Lensjø
authors.affiliation: Institute of Basic Medical Sciences, and.|Center for Integrative Neuroplasticity, University of Oslo, 0370 Oslo, Norway.
authors.forename: Mikkel Elle
authors.identifier: 0000-0002-4262-5549
authors.initials: ME
authors.lastname: Lepperød
authors.affiliation: Department of Biosciences.
authors.forename: Gunnar
authors.identifier: 0000-0003-4529-5239
authors.initials: G
authors.lastname: Dick
authors.affiliation: Institute of Basic Medical Sciences, and.|Center for Integrative Neuroplasticity, University of Oslo, 0370 Oslo, Norway.
authors.forename: Torkel
authors.identifier: 0000-0002-0928-3487
authors.initials: T
authors.lastname: Hafting
authors.affiliation: Department of Biosciences, marianne.fyhn@ibv.uio.no.|Center for Integrative Neuroplasticity, University of Oslo, 0370 Oslo, Norway.
authors.forename: Marianne
authors.initials: M
authors.lastname: Fyhn
mesh_terms: D000375:Aging / Q000502:physiology; D000818:Animals; D004567:Electrodes, Implanted; D004569:Electroencephalography; D055724:Electrophysiological Phenomena / Q000502:physiology; D005109:Extracellular Matrix / Q000502:physiology*; D065818:Gamma Rhythm / Q000502:physiology*; D008297:Male; D009415:Nerve Net / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D010775:Photic Stimulation; D051381:Rats; D020318:Rats, Long-Evans; D013569:Synapses / Q000502:physiology; D015349:Vision, Monocular; D014793:Visual Cortex / Q000254:growth & development / Q000502:physiology
keywords: activity-dependent plasticity; cortical plasticity; gamma; inhibition; local field potential; perineuronal nets