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The Journal of Neuroscience, February 4, 2009, 29(5):1300-1311; doi:10.1523/JNEUROSCI.5446-08.2009

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Development/Plasticity/Repair
Random Walk Behavior of Migrating Cortical Interneurons in the Marginal Zone: Time-Lapse Analysis in Flat-Mount Cortex

Daisuke H. Tanaka,^1,2 Mitsutoshi Yanagida,¹ Yan Zhu,¹ Sakae Mikami,³ Takashi Nagasawa,³ Jun-ichi Miyazaki,⁴ Yuchio Yanagawa,⁵ Kunihiko Obata,⁶ and Fujio Murakami¹

¹Graduate School of Frontier Biosciences, Osaka University, Osaka 565-0871, Japan, ²Department of Anatomy, Keio University School of Medicine, Tokyo 160-8582, Japan, ³Department of Medical Systems Control, Institute for Frontier Medical Sciences, Kyoto University, Kyoto 606-8507, Japan, ⁴Division of Stem Cell Regulation Research, Osaka University Medical School, Osaka 565-0871, Japan, ⁵Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi 371-8511, Japan, and ⁶Neural Circuit Mechanism Group, Brain Science Institute, RIKEN, Wako 351-0198, Japan

Correspondence should be addressed to Fujio Murakami, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 1-3, Suita, Osaka 565-0871, Japan. Email: murakami{at}fbs.osaka-u.ac.jp

Migrating neurons are thought to travel from their origin near the ventricle to distant territories along stereotypical pathways by detecting environmental cues in the extracellular milieu. Here, we report a novel mode of neuronal migration that challenges this view. We performed long-term, time-lapse imaging of medial ganglionic eminence (MGE)-derived cortical interneurons tangentially migrating in the marginal zone (MZ) in flat-mount cortices. We find that they exhibit a diverse range of behaviors in terms of the rate and direction of migration. Curiously, a predominant population of these neurons repeatedly changes its direction of migration in an unpredictable manner. Trajectories of migration vary from one neuron to another. The migration of individual cells lasts for long periods, sometimes up to 2 d. Theoretical analyses reveal that these behaviors can be modeled by a random walk. Furthermore, MZ cells migrate from the cortical subventricular zone to the cortical plate, transiently accumulating in the MZ. These results suggest that MGE-derived cortical interneurons, once arriving at the MZ, are released from regulation by guidance cues and initiate random walk movement, which potentially contributes to their dispersion throughout the cortex.

Key words: cerebral cortex; GABAergic interneuron; migration; random walk; time-lapse imaging; marginal zone

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Received Nov. 11, 2008; accepted Dec. 16, 2008.

Correspondence should be addressed to Fujio Murakami, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 1-3, Suita, Osaka 565-0871, Japan. Email: murakami{at}fbs.osaka-u.ac.jp

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