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The Journal of Neuroscience, March 19, 2008, 28(12):3076-3089; doi:10.1523/JNEUROSCI.0172-08.2008

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Behavioral/Systems/Cognitive
Differential Columnar Processing in Local Circuits of Barrel and Insular Cortices

Hajime Sato, * Yasushi Shimanuki, * Mitsuru Saito, * Hiroki Toyoda, * Takashi Nokubi, Yoshinobu Maeda, Takashi Yamamoto, and Youngnam Kang

Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka 565-0871, Japan

Correspondence should be addressed to Dr. Youngnam Kang, Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, 1-8, Yamadaoka, Suita, Osaka 565-0871, Japan. Email: kang{at}dent.osaka-u.ac.jp

The columnar organization is most apparent in the whisker barrel cortex but seems less apparent in the gustatory insular cortex. We addressed here whether there are any differences between the two cortices in columnar information processing by comparing the spatiotemporal patterns of excitation spread in the two cortices using voltage-sensitive dye imaging. In contrast to the well known excitation spread in the horizontal direction in layer II/III induced in the barrel cortex by layer IV stimulation, the excitation caused in the insular cortex by stimulation of layer IV spread bidirectionally in the vertical direction into layers II/III and V/VI, displaying a columnar image pattern. Bicuculline or picrotoxin markedly extended the horizontal excitation spread in layer II/III in the barrel cortex, leading to a generation of excitation in the underlying layer V/VI, whereas those markedly increased the amplitude of optical responses throughout the whole column in the insular cortex, subsequently widening the columnar image pattern. Such synchronous activities as revealed by the horizontal and vertical excitation spreads were consistently induced in the barrel and insular cortices, respectively, even by stimulation of different layers with varying intensities. Thus, a unique functional column existed in the insular cortex, in which intracolumnar communication between the superficial and deep layers was prominent, and GABAA action is involved in the inhibition of the intracolumnar communication in contrast to its involvement in intercolumnar lateral inhibition in the barrel cortex. These results suggest that the columnar information processing may not be universal across the different cortical areas.

Key words: barrel cortex; insular cortex; lateral inhibition; functional column; GABAA receptor; voltage-sensitive dye


Received July 12, 2007; revised Feb. 4, 2008; accepted Feb. 4, 2008.

Correspondence should be addressed to Dr. Youngnam Kang, Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, 1-8, Yamadaoka, Suita, Osaka 565-0871, Japan. Email: kang{at}dent.osaka-u.ac.jp




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