Inhibitory effect of mouse neocortex layer I on the underlying cellular network

Eur J Neurosci. 2003 Nov;18(10):2751-9. doi: 10.1111/j.1460-9568.2003.03016.x.

Abstract

The mammalian cortical layer I is a convergence site for axons of sub- and intracortical origin, and the apical dendritic tufts of pyramidal neurons. A prominent feature of layer I is an extensive plexus of inhibitory axons, which originate from stellate cells in all cortical laminae. The role of this inhibitory projection in the activity of cortical networks has yet to be determined. We investigated the degree to which inhibitory inputs within layer I affect the activity of the underlying cellular network. Field potentials (FPs) were recorded in layer II/III. Focal application of the GABAA blocker picrotoxin in layer I above the recording pipette or the removal of layer I resulted in larger FP amplitudes for stimulations at control-equal intensities. When inhibition was partially blocked, the removal of layer I caused a significant reduction in the threshold stimulus intensity required for generating epileptiform events, and a rise in the propagation velocity of these events. Immunocytochemistry for chemical markers of interneurons proved that the inhibitory input to layer I is predominantly somatostatin immunoreactive (SM-ir), such that layer I contains approximately one-third of all SM-ir axons in the cortex. Calretinin-immunoreactive axons were also present in layer I at a lower density. We conclude that the impact of layer I on the cortical cellular network includes a significant inhibitory component. This inhibition confers a moderate restraining influence, and its removal increases the excitability of cortical circuits, but not sufficiently to induce epileptic phenomena.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / metabolism
  • Calbindin 2
  • Dendrites / metabolism
  • Dissection
  • Dose-Response Relationship, Radiation
  • Electric Conductivity
  • Electric Stimulation
  • Evoked Potentials / drug effects
  • Evoked Potentials / physiology*
  • GABA Antagonists / pharmacology
  • Immunohistochemistry
  • In Vitro Techniques
  • Interneurons / cytology
  • Interneurons / metabolism
  • Male
  • Mice
  • Neocortex / anatomy & histology
  • Neocortex / drug effects
  • Neocortex / physiology*
  • Nerve Net / cytology
  • Nerve Net / drug effects
  • Nerve Net / physiology*
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology*
  • Parvalbumins / metabolism
  • Picrotoxin / pharmacology
  • S100 Calcium Binding Protein G / metabolism
  • Somatostatin / metabolism

Substances

  • Calb2 protein, mouse
  • Calbindin 2
  • GABA Antagonists
  • Parvalbumins
  • S100 Calcium Binding Protein G
  • Picrotoxin
  • Somatostatin