Journal of Neuroscience, Vol 5, 3246-3260, Copyright © 1985 by Society for Neuroscience
Vertical organization of gamma-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex
J DeFelipe and EG Jones
Light and electron microscopic methods were used to examine the neurons in
the monkey cerebral cortex labeled autoradiographically following the
uptake and transport of [3H]-gamma-aminobutyric acid (GABA). Nonpyramidal
cell somata in the sensory-motor areas and primary visual area (area 17)
were labeled close to the injection site and at distances of 1 to 1.5 mm
beyond the injection site, indicating labeling by retrograde axoplasmic
transport. This labeling occurred preferentially in the vertical dimension
of the cortex. Prior injections of colchicine, an inhibitor of axoplasmic
transport, abolished all labeling of somata except those within the
injection site. In each area, injections of superficial layers (I to III)
produced labeling of clusters of cell somata in layer V, and injections of
the deep layers (V and VI) produced labeling of clusters of cell somata in
layers II and III. In area 17, injections of the superficial layers
produced dense retrograde cell labeling in three bands: in layers IVC, VA,
and VI. Vertically oriented chains of silver grains linked the injection
sites with the resulting labeled cell clusters. In all areas, the labeling
of cells in the horizontal dimension, i.e., on each side of an injection,
was insignificant. Electron microscopic examination of labeled neurons
confirms that the neurons labeled at a distance from an injection site are
nonpyramidal neurons, many with somata so small that they would be mistaken
for neuroglial cells light microscopically. They receive few axosomatic
synapses, most of which have symmetric membrane thickenings. The vertical
chains of silver grains overlie neuronal processes identifiable as both
dendrites and myelinated axons, but unmyelinated axons may also be
included. The clusters of [3H]GABA-labeled cells are joined to one another
and to adjacent unlabeled cells by many junctional complexes, including
puncta adherentia and multi-lamellar cisternal complexes. We conclude that
groups of GABA-transporting neurons are likely to use GABA as a transmitter
and form an inhibitory, bidirectional system of connections that join
together cells in superficial and deep layers of functional cortical
columns; intrinsic, horizontal GABAergic connections are either far less
significant in the organization of the cerebral cortex or are not labeled
by this method.(ABSTRACT TRUNCATED AT 400 WORDS)
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