On the nature of the intrinsic connectivity of the cat motor cortex: evidence for a recurrent neural network topology

J Neurophysiol. 2009 Oct;102(4):2131-41. doi: 10.1152/jn.91319.2008. Epub 2009 Jul 22.

Abstract

The details and functional significance of the intrinsic horizontal connections between neurons in the motor cortex (MCx) remain to be clarified. To further elucidate the nature of this intracortical connectivity pattern, experiments were done on the MCx of three cats. The anterograde tracer biocytin was ejected iontophoretically in layers II, III, and V. Some 30-50 neurons within a radius of approximately 250 microm were thus stained. The functional output of the motor cortical point at which biocytin was injected, and of the surrounding points, was identified by microstimulation and electromyographic recordings. The axonal arborizations of the stained neurons were traced under camera lucida. The axon collaterals were extensive, reaching distances of <or=7 mm from the injection site. More importantly, the axonal branches were studded all along their course with boutons. The vast majority of boutons formed synaptic contacts on the target cells as identified by electron microscopy. The majority of these boutons made asymmetric (type I, excitatory) synapses mainly on dendritic spines. The bouton density decreased approximately monotonically with distance from the center of the injection. Cluster analysis, lagged covariance analysis, and eigenvalue decomposition showed the bouton distribution map to be unimodal. Superposition of the synaptic bouton distribution map and the motor output map revealed that motor cortical neurons don't make point-to-point connections but rather bind together the representations of a variety of muscles within a large neighborhood. This recurrent-network type connectivity strongly supports the hypothesis that the MCx controls the musculature in an integrated manner.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / physiology
  • Axons / ultrastructure
  • Cats
  • Cluster Analysis
  • Dendritic Spines / physiology
  • Dendritic Spines / ultrastructure
  • Electric Stimulation
  • Electromyography
  • Lysine / analogs & derivatives
  • Male
  • Microelectrodes
  • Microscopy, Electron
  • Motor Cortex / cytology
  • Motor Cortex / physiology*
  • Motor Cortex / ultrastructure
  • Multivariate Analysis
  • Muscle, Skeletal / innervation
  • Muscle, Skeletal / physiology
  • Neural Pathways / cytology
  • Neural Pathways / physiology
  • Neural Pathways / ultrastructure
  • Neuronal Tract-Tracers
  • Neurons / cytology
  • Neurons / physiology*
  • Neurons / ultrastructure
  • Presynaptic Terminals / physiology
  • Presynaptic Terminals / ultrastructure
  • Pyramidal Cells / cytology
  • Pyramidal Cells / physiology
  • Pyramidal Cells / ultrastructure
  • Synapses / physiology
  • Synapses / ultrastructure

Substances

  • Neuronal Tract-Tracers
  • biocytin
  • Lysine