Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat

Cereb Cortex. 1997 Oct-Nov;7(7):605-18. doi: 10.1093/cercor/7.7.605.

Abstract

The topography of lateral excitatory and lateral inhibitory connections was studied in relation to orientation maps obtained in areas 17 and 18. Small iontophoretic injections of biocytin were delivered to the superficial layers in regions where orientation selectivity had been mapped using electrode recordings of single- and multi-unit activity from various cortical depths. Biocytin revealed extensive patchy axonal projections of up to 3.5 mm in both areas while labelled somata occurred chiefly at the injection site, indicating that the labelling was primarily anterograde. Two types of boutons could be clearly distinguished: (i) putative excitatory boutons either en passant or having a short stalk and (ii) inhibitory boutons which were invariably of the basket-type. Three-dimensional reconstructions of all labelled boutons showed that the excitatory and the inhibitory networks had a distinctively different relationship to orientation maps. The overall distribution of connections showed that 53-59% of excitatory and 46-48% of inhibitory connections were at iso-orientation, +/-30 degrees; oblique-orientation, +/-(30-60) degrees, was shown by 30% of excitatory and 28-39% of inhibitory connections; cross-orientation was shown by 11-17% of excitatory and 15-24% of inhibitory connections. Although excitatory patches occupied mainly iso-orientation locations, interpatch regions representing chiefly non-iso-orientations (oblique + cross orientation) were also innervated. There was considerable overlap between the excitatory and inhibitory network. Nonetheless, inhibitory connections were more common than excitatory connections with non-iso-orientation locations. There was no significant difference between the orientation topography of area 17 and area 18 projections. The results suggest that in general the lateral connectivity system is not orientation specific, but shows a moderate iso-orientation preference for excitation and an even weaker iso-orientation preference for inhibition. The broad orientation spectrum of lateral connections could provide the basis for mechanisms that requiring different orientations, as for example in detecting orientation discontinuities.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axonal Transport
  • Axons / physiology
  • Axons / ultrastructure
  • Brain Mapping*
  • Cats
  • Electrophysiology
  • Lysine / analogs & derivatives
  • Models, Anatomic
  • Nerve Fibers, Myelinated / physiology
  • Nerve Fibers, Myelinated / ultrastructure
  • Neurons / cytology*
  • Neurons / physiology*
  • Orientation
  • Pyramidal Cells / cytology
  • Pyramidal Cells / physiology
  • Visual Cortex / anatomy & histology*
  • Visual Cortex / physiology*

Substances

  • biocytin
  • Lysine