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A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neocortex

Nature Neuroscience volume 10, pages 1141–1150 (2007)Cite this article

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Abstract

The amygdaloid complex consists of diverse nuclei that belong to distinct functional systems, yet many issues about its development are poorly understood. Here, we identify a stream of migrating cells that form specific amygdaloid nuclei in mice. In utero electroporation showed that this caudal amygdaloid stream (CAS) originated in a unique domain at the caudal telencephalic pole that is contiguous with the dorsal pallium, which was previously thought to generate only neocortical cells. The CAS and the neocortex share mechanisms for specification (transcription factors Tbr1, Lhx2 and Emx1/2) and migration (reelin and Cdk5). Reelin, a critical cue for migration in the neocortex, and Cdk5, which is specifically required for migration along radial glia in the neocortex, were both selectively required for the normal migration of the CAS, but not for that of other amygdaloid nuclei. This is first evidence of a dorsal pallial contribution to the amygdala, demonstrating a developmental and mechanistic link between the amygdala and the neocortex.

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Figure 1: A stream of amygdaloid cells from the caudal telencephalon.
Figure 2: In utero electroporation identifies a unique caudal origin for the CAS.
Figure 3: Multiple pallial markers identify the CAS and the nLOT2 emerging from the caudal telencephalic neuroepithelium.
Figure 4: The CAS originates in the dorsal pallium.
Figure 5: The CAS migrates in a reelin-free corridor.
Figure 6: The CAS migration is abnormal in the reeler mutant.
Figure 7: Radial glia and the CAS trajectory.
Figure 8: Migration of the CAS requires Cdk5.

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  • 19 August 2007

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Acknowledgements

We thank R. Kageyama, Y. Nakagawa, F. D. Porter, T. Rabbitts, C. Ragsdale, E. Grove and Y. Zhao for gifts of plasmid DNA; F. D. Porter for the Lhx2 mutant breeding pairs; M. Frotscher for the gift of reeler mutant tissue for preliminary experiments; and V. Vaidya, M. Benekareddy and A. Nair for critical comments on the manuscript. The Rat-401 monoclonal antibody to Nestin, developed by S. Hockfield, was obtained from the Developmental Studies Hybridoma Bank and was developed under the auspices of the US National Institute of Child Health and Human Development and maintained by The University of Iowa. We also thank the Tata Institute of Fundamental Research Animal House staff for excellent support. This work was supported by a Wellcome Trust Senior Fellowship (056684/Z/99/Z) and a Swarnajayanti Fellowship (Dept. of Science and Technology, Govt. of India) to S.T. and a Kanwal Rekhi Career Development Award (Tata Institute of Fundamental Research Endowment Fund) to B.S. and P.H.

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Authors and Affiliations

  1. Department of Biological Sciences, B–304, Tata Institute of Fundamental Research, Homi Bhabha Road, Colaba, Mumbai, 400005, India

    Ryan Remedios, Dhananjay Huilgol, Bhaskar Saha, Padmanabhan Hari, Lahar Bhatnagar & Shubha Tole

  2. Department of Pathology, University of Washington, Seattle, 98195-7270, Washington, USA

    Thomas Kowalczyk & Robert F Hevner

  3. Center on Human Development and Disability, University of Washington, Seattle, 98195-7270, Washington, USA

    Robert F Hevner

  4. Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, 98195-7270, Washington, USA

    Robert F Hevner

  5. Laboratory for Vertebrate Body Plan, Center for Developmental Biology, 2-2-3 Minatojima-minamimachi, Chuo-ku, RIKEN, Kobe, 650-0047, Japan

    Yoko Suda & Shinichi Aizawa

  6. Laboratory for Developmental Neurobiology, Brain Science Institute, RIKEN, Saitama, 351-0198, Japan

    Toshio Ohshima

  7. Department of Life Science and Medical Bio-Science, Waseda University, 3-4-1 Okubo Shinjuku-ku, Tokyo, 169-8555, Japan

    Toshio Ohshima

  8. Max-Planck Institute of Biophysical Chemistry, Am Fassberg 11, Göttingen, D-37077, Germany

    Anastassia Stoykova

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Contributions

R.R., D.H., B.S., P.H. and L.B. carried out the experiments. R.R., D.H. and S.T. analyzed the data. S.T. supervised the project and wrote the paper. Mutant mouse tissue was provided by T.K. and R.F.H. (Tbr1 mutant and preliminary data), Y.S. and S.A. (Emx1 and Emx1/2 double mutants), T.O. (Cdk5 mutant) and A.S. (Emx2 and reeler mutants).

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Correspondence to Shubha Tole.

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Remedios, R., Huilgol, D., Saha, B. et al. A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neocortex. Nat Neurosci 10, 1141–1150 (2007). https://doi.org/10.1038/nn1955

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