The Journal of Neuroscience, February 15, 1998, 18(4):1505-1527
Prenatal Development of Layer-Specific Local Circuits in Primary
Visual Cortex of the Macaque Monkey
Edward M.
Callaway
Systems Neurobiology Laboratory, The Salk Institute for Biological
Studies, La Jolla, California 92037
Previous studies have demonstrated that axonal arbors specific for
the four main cortical layers 
2/3, 4, 5, and 6 develop precisely from the outset using activity-independent cues. In macaque
primary visual cortex (V1), layer 2/3 is subdivided into layers named
2/3A, 3B, 4A, and 4B, and layer 4 is subdivided into 4C
and 4C
.
Individual neurons in V1 of mature macaques have axonal arbors that are
highly specific for these sublayers. We have studied the prenatal
development of laminar and sublaminar specificity of local circuits in
macaque V1. Two-hundred thirty-eight neurons were labeled
intracellularly in living brain slices prepared from V1 of five
prenatal macaque monkeys aged 100 to 145 d postconception (E100-E145). Axonal and dendritic arbors of labeled neurons were reconstructed to assess their relationships to the cortical layers. We
find that developing spiny neurons in layers 2-4B and layer 5 specifically target superficial and deep layers without forming "incorrect" branches in layer 4C. Similarly, layer 6 pyramidal neurons that target layer 4C do not form "incorrect" branches in
layer 5. These results indicate that specific projections to the main
cortical layers develop with a high degree of selectivity, as in other
species. However, the development of sublayer-specific projections was
not always precise from the outset. Unlike postnatal animals, axons of
some prenatal layer 4C spiny neurons branch in layer 4B. At similar
ages, many pyramidal neurons in the upper half of layer 6 have axonal
branches in layer 4C as well as 4C; these projections are
specific for 4C in more mature animals. Also, there is similar
"exuberance" in axonal arbors of other layer 6 cell types.
Transient projections were also observed in the subplate and to the
white matter for cells from all layers, except 4C. These
observations indicate that at least some sublayer-specific projections
emerge by elimination of exuberant axonal branches and suggest that
they may use activity-dependent mechanisms to identify "correct"
target layers. Such cues could be provided by laminar differences in
the patterns of spontaneous prenatal activity in the
retino-geniculo-cortical network.
Key words:
development; local circuits; primate; macaque; visual
cortex; V1; area 17; striate cortex
Copyright © 1998 Society for Neuroscience 0270-6474/98/1841505-23$05.00/0
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