Synaptogenesis of Electrical and GABAergic Synapses of Fast-Spiking Inhibitory Neurons in the Neocortex

J Neurosci. 2011 Jul 27;31(30):10767-75. doi: 10.1523/JNEUROSCI.6655-10.2011.

Abstract

Parvalbumin-expressing fast-spiking (FS) cells are interconnected via GABAergic and electrical synapses and represent a major class of inhibitory interneurons in the neocortex. Synaptic connections among FS cells are critical for regulating network oscillations in the mature neocortex. However, it is unclear whether synaptic connections among FS interneurons also play a central role in the generation of patterned neuronal activity in the immature brain, which is thought to underlie the formation of neocortical circuits. Here, we investigated the developmental time course of synaptogenesis of FS cell in mouse visual cortex. In layer 5/6 (L5/6), we recorded from two or three FS and/or pyramidal (PYR) neurons to study the development of electrical and chemical synaptic interactions from postnatal day 3 (P3) to P18. We detected no evidence for functional connectivity for FS-FS or FS-PYR pairs at P3-P4. However, by P5-P6, we found that 20% of FS pairs were electrically coupled, and 24% of pairs were connected via GABAergic synapses; by P15-P18, 42% of FS pairs had established functional electrical synapses, and 47% of FS pairs were connected via GABAergic synapses. FS cell GABAergic inhibition of pyramidal cells showed a similar developmental time line, but no electrical coupling was detected for FS-PYR pairs. We found that synaptogenesis of electrical and GABAergic connections of FS cells takes place in the same period. Together, our results suggest that chemical and electrical connections among FS cells can contribute to patterned neocortical activity only by the end of the first postnatal week.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / genetics
  • Action Potentials / physiology*
  • Age Factors
  • Analysis of Variance
  • Animals
  • Animals, Newborn
  • Electrical Synapses / genetics
  • Electrical Synapses / physiology*
  • Glutamate Decarboxylase / genetics
  • Green Fluorescent Proteins / genetics
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / genetics
  • Inhibitory Postsynaptic Potentials / physiology
  • Mice
  • Mice, Transgenic
  • Neocortex / cytology*
  • Neocortex / growth & development
  • Neural Inhibition / physiology*
  • Parvalbumins / metabolism
  • Pyramidal Cells / physiology
  • Signal Transduction / genetics
  • gamma-Aminobutyric Acid / genetics
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Parvalbumins
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • gamma-Aminobutyric Acid
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1