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Removal of Perineuronal Nets Unlocks Juvenile Plasticity Through Network Mechanisms of Decreased Inhibition and Increased Gamma Activity
- Source :
- The Journal of Neuroscience. 37:1269-1283
- Publication Year :
- 2016
- Publisher :
- Society for Neuroscience, 2016.
-
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.SIGNIFICANCE STATEMENTEmerging evidence suggests a role for perineuronal nets (PNNs) in learning and regulation of plasticity, but the underlying mechanisms remain unresolved. Here, we used chronicin vivoextracellular 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.
- Subjects :
- Male
0301 basic medicine
Aging
Population
Biology
Inhibitory postsynaptic potential
03 medical and health sciences
0302 clinical medicine
Vision, Monocular
Neuroplasticity
Metaplasticity
Animals
Gamma Rhythm
Rats, Long-Evans
education
Research Articles
Visual Cortex
education.field_of_study
Neuronal Plasticity
General Neuroscience
Perineuronal net
Electroencephalography
Long-term potentiation
Electrodes, Implanted
Electrophysiological Phenomena
Extracellular Matrix
Rats
Monocular deprivation
030104 developmental biology
Synapses
Activity-dependent plasticity
Nerve Net
Neuroscience
Photic Stimulation
030217 neurology & neurosurgery
Subjects
Details
- ISSN :
- 15292401 and 02706474
- Volume :
- 37
- Database :
- OpenAIRE
- Journal :
- The Journal of Neuroscience
- Accession number :
- edsair.doi.dedup.....0250301b9faac3641d0972bc534b76ed