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Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period.

Publication ,  Journal Article
Chattopadhyaya, B; Di Cristo, G; Higashiyama, H; Knott, GW; Kuhlman, SJ; Welker, E; Huang, ZJ
Published in: J Neurosci
October 27, 2004

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.

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Published In

J Neurosci

DOI

EISSN

1529-2401

Publication Date

October 27, 2004

Volume

24

Issue

43

Start / End Page

9598 / 9611

Location

United States

Related Subject Headings

  • gamma-Aminobutyric Acid
  • Visual Cortex
  • Vision, Ocular
  • Tissue Culture Techniques
  • Time Factors
  • Tetrodotoxin
  • Synapses
  • Sensory Deprivation
  • Recombinant Fusion Proteins
  • Pyramidal Cells
 

Citation

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Chattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G. W., Kuhlman, S. J., Welker, E., & Huang, Z. J. (2004). Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci, 24(43), 9598–9611. https://doi.org/10.1523/JNEUROSCI.1851-04.2004
Chattopadhyaya, Bidisha, Graziella Di Cristo, Hiroyuki Higashiyama, Graham W. Knott, Sandra J. Kuhlman, Egbert Welker, and Z Josh Huang. “Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period.J Neurosci 24, no. 43 (October 27, 2004): 9598–9611. https://doi.org/10.1523/JNEUROSCI.1851-04.2004.
Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, et al. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci. 2004 Oct 27;24(43):9598–611.
Chattopadhyaya, Bidisha, et al. “Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period.J Neurosci, vol. 24, no. 43, Oct. 2004, pp. 9598–611. Pubmed, doi:10.1523/JNEUROSCI.1851-04.2004.
Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci. 2004 Oct 27;24(43):9598–9611.

Published In

J Neurosci

DOI

EISSN

1529-2401

Publication Date

October 27, 2004

Volume

24

Issue

43

Start / End Page

9598 / 9611

Location

United States

Related Subject Headings

  • gamma-Aminobutyric Acid
  • Visual Cortex
  • Vision, Ocular
  • Tissue Culture Techniques
  • Time Factors
  • Tetrodotoxin
  • Synapses
  • Sensory Deprivation
  • Recombinant Fusion Proteins
  • Pyramidal Cells