Experience and Activity-Dependent Maturation of Perisomatic GABAergic Innervation in Primary Visual Cortex during a Postnatal Critical Period

The neocortical GABAergic network consists of diverse interneuron cell types that display distinct physiological properties and target their innervations to subcellular compartments of principal neurons. Inhibition directed toward the soma and proximal dendrites is crucial in regulating the output o...

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Bibliographic Details
Published in:The Journal of neuroscience 2004-10, Vol.24 (43), p.9598-9611
Main Authors: Chattopadhyaya, Bidisha, Di Cristo, Graziella, Higashiyama, Hiroyuki, Knott, Graham W, Kuhlman, Sandra J, Welker, Egbert, Huang, Z. Josh
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Animals
Chromosomes, Artificial, Bacterial
Development/Plasticity/Repair
DNA Repair
gamma-Aminobutyric Acid - physiology
Glutamate Decarboxylase - genetics
Green Fluorescent Proteins - genetics
Interneurons - physiology
Isoenzymes - genetics
Mice
Mice, Transgenic
Neural Inhibition - physiology
Neuronal Plasticity - physiology
Presynaptic Terminals - physiology
Pyramidal Cells - physiology
Recombinant Fusion Proteins
Sensory Deprivation - physiology
Synapses - physiology
Tetrodotoxin - pharmacology
Time Factors
Tissue Culture Techniques
Vision, Ocular - physiology
Visual Cortex - growth & development
Visual Cortex - physiology
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Summary:The neocortical GABAergic network consists of diverse interneuron cell types that display distinct physiological properties and target their innervations to subcellular compartments of principal neurons. Inhibition directed toward the soma and proximal dendrites is crucial in regulating the output of pyramidal neurons, but the development of perisomatic innervation is poorly understood because of the lack of specific synaptic markers. In the primary visual cortex, for example, it is unknown whether, and to what extent, the formation and maturation of perisomatic synapses are intrinsic to cortical circuits or are regulated by sensory experience. Using bacterial artificial chromosome transgenic mice that label a defined class of perisomatic synapses with green fluorescent protein, here we show that perisomatic innervation developed during a protracted postnatal period after eye opening. Maturation of perisomatic innervation was significantly retarded by visual deprivation during the third, but not the fifth, postnatal week, implicating an important role for sensory input. To examine the role of cortical intrinsic mechanisms, we developed a method to visualize perisomatic synapses from single basket interneurons in cortical organotypic cultures. Characteristic perisomatic synapses formed through a stereotyped process, involving the extension of distinct terminal branches and proliferation of perisomatic boutons. Neuronal spiking in organotypic cultures was necessary for the proliferation of boutons and the extension, but not the maintenance, of terminal branches. Together, our results suggest that although the formation of perisomatic synapses is intrinsic to the cortex, visual experience can influence the maturation and pattern of perisomatic innervation during a postnatal critical period by modulating the level of neural activity within cortical circuits.
ISSN:0270-6474
1529-2401
DOI:10.1523/JNEUROSCI.1851-04.2004