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Cerebral Cortex Advance Access originally published online on December 4, 2008
Cerebral Cortex 2009 19(8):1915-1928; doi:10.1093/cercor/bhn219
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© 2008 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Enriched Expression of Serotonin 1B and 2A Receptor Genes in Macaque Visual Cortex and their Bidirectional Modulatory Effects on Neuronal Responses

Akiya Watakabe1,2, Yusuke Komatsu1, Osamu Sadakane3, Satoshi Shimegi3, Toru Takahata1, Noriyuki Higo4, Shiro Tochitani1,2,7, Tsutomu Hashikawa5, Tomoyuki Naito3, Hironobu Osaki3, Hiroshi Sakamoto3, Masahiro Okamoto3, Ayako Ishikawa3, Shin-ichiro Hara3, Takafumi Akasaki3, Hiromichi Sato3 and Tetsuo Yamamori1,2,6

1 Division of Brain Biology, National Institute for Basic Biology, 38 Nishigonaka Myodaiji, Okazaki 444-8585, Japan, 2 Department of Basic Biology, Graduate University for Advanced Studies, 38 Nishigonaka Myodaiji, Okazaki 444-8585, Japan, 3 Laboratory of Cognitive and Behavioral Neuroscience, Graduate School of Medicine, Osaka University, Toyonaka 560-0043, Japan, 4 System Neuroscience Group, Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, Umezono 1-1-1, Tsukuba 305-8568, Japan, 5 Laboratory for Neural Architecture, Brain Science Institute, RIKEN, Wako 351-0198, Japan, 6 National Institute for Physiological Sciences, 38 Nishigonaka Myodaiji, Okazaki 444-8585, Japan

Address correspondence to Tetsuo Yamamori Dr. Sci., Division of Brain Biology, National Institute for Basic Biology, 38 Nishigonaka Myodaiji, Okazaki 444-8585, Japan. Email: yamamori{at}nibb.ac.jp.

To study the molecular mechanism how cortical areas are specialized in adult primates, we searched for area-specific genes in macaque monkeys and found striking enrichment of serotonin (5-hydroxytryptamine, 5-HT) 1B receptor mRNA, and to a lesser extent, of 5-HT2A receptor mRNA, in the primary visual area (V1). In situ hybridization analyses revealed that both mRNA species were highly concentrated in the geniculorecipient layers IVA and IVC, where they were coexpressed in the same neurons. Monocular inactivation by tetrodotoxin injection resulted in a strong and rapid (<3 h) downregulation of these mRNAs, suggesting the retinal activity dependency of their expression. Consistent with the high expression level in V1, clear modulatory effects of 5-HT1B and 5-HT2A receptor agonists on the responses of V1 neurons were observed in in vivo electrophysiological experiments. The modulatory effect of the 5-HT1B agonist was dependent on the firing rate of the recorded neurons: The effect tended to be facilitative for neurons with a high firing rate, and suppressive for those with a low firing rate. The 5-HT2A agonist showed opposite effects. These results suggest that this serotonergic system controls the visual response in V1 for optimization of information processing toward the incoming visual inputs.

Key Words: 5-HT • activity-dependent • area-specific • monocular deprivation • primate • visual cortex

7 Current address: Anatomy and Developmental Neurobiology, Institute of Health Biosciences, University of Tokushima Graduate School, 3-18-15 Kuramotochou, Tokushima 770-8503, Japan.

Akiya Watakabe, Yusuke Komatsu, and Osamu Sadakane contributed equally to this work.


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