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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 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.

Pubmed ID: 15509747

Authors

  • Chattopadhyaya B
  • Di Cristo G
  • Higashiyama H
  • Knott GW
  • Kuhlman SJ
  • Welker E
  • Huang ZJ

Journal

The Journal of neuroscience : the official journal of the Society for Neuroscience

Publication Data

October 27, 2004

Associated Grants

  • Agency: NEI NIH HHS, Id: R01 EY13564-01

Mesh Terms

  • Action Potentials
  • Animals
  • Chromosomes, Artificial, Bacterial
  • DNA Repair
  • Glutamate Decarboxylase
  • Green Fluorescent Proteins
  • Interneurons
  • Isoenzymes
  • Mice
  • Mice, Transgenic
  • Neural Inhibition
  • Neuronal Plasticity
  • Presynaptic Terminals
  • Pyramidal Cells
  • Recombinant Fusion Proteins
  • Sensory Deprivation
  • Synapses
  • Tetrodotoxin
  • Time Factors
  • Tissue Culture Techniques
  • Vision, Ocular
  • Visual Cortex
  • gamma-Aminobutyric Acid