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The Journal of Neuroscience, February 15, 2003, 23(4):1372

Honeycomb-Like Mosaic at the Border of Layers 1 and 2 in the Cerebral Cortex

Noritaka Ichinohe¹, Fumino Fujiyama², Takeshi Kaneko², and Kathleen S. Rockland¹

¹ Laboratory for Cortical Organization and Systematics, RIKEN, Brain Science Institute, Wako, Saitama 351-0198, Japan, and ² Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan

In this report, we present evidence of a small-scale modularity (<100 µm) at the border of layers 1 and 2 in neocortical areas. The modularity is best seen in tangential sections, with double-labeling immunohistochemistry to reveal overlapping or complementary relationships of different markers. The pattern is overall like a reticulum or mosaic but is described as a "honeycomb," in which the walls and hollows are composed of distinct afferent and dendritic systems. We demonstrate the main components of the honeycomb in rat visual cortex. These are as follows: (1) zinc-enriched, corticocortical terminations in the walls, and in the hollows, thalamocortical terminations (labeled by antibody against vesicular glutamate transporter 2 and by cytochrome oxidase); (2) parvalbumin-dense neuropil in the walls that partly colocalizes with elevated levels of glutamate receptors 2/3, NMDAR receptor 1, and calbindin; and (3) dendritic subpopulations preferentially situated within the walls (dendrites of layer 2 neurons) or hollows (dendrites of deeper neurons in layers 3 and 5). Because the micromodularity is restricted to layers 2 and 1b, without extending into layer 3, this may be another indication of a laminar-specific substructure at different spatial scales within cortical columns. The suggestion is that corticocortical and thalamocortical terminations constitute parallel circuits at the level of layer 2, where they are segregated in association with distinct dendritic systems. Results from parvalbumin staining show that the honeycomb mosaic is not limited to rat visual cortex but can be recognized at the layer 1-2 border in other areas and species.

Key words: columnar organization; zinc-enriched corticocortical terminals; thalamocortical terminals; parvalbumin; dendritic minicolumn; rat visual cortex; cytochrome oxidase

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Copyright © 2003 Society for Neuroscience  0270-6474/03/2341372-11$05.00/0

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