Dual midbrain and forebrain origins of thalamic inhibitory interneurons

Author:

Jager Polona1ORCID,Moore Gerald23,Calpin Padraic4,Durmishi Xhuljana1,Salgarella Irene1ORCID,Menage Lucy1,Kita Yoshiaki5,Wang Yan5,Kim Dong Won6,Blackshaw Seth6,Schultz Simon R2ORCID,Brickley Stephen3,Shimogori Tomomi5,Delogu Alessio1ORCID

Affiliation:

1. Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom

2. Department of Bioengineering, Imperial College London, London, United Kingdom

3. Department of Life Sciences and Centre for Neurotechnology, Imperial College London, London, United Kingdom

4. Department of Physics and Astronomy, University College London, London, United Kingdom

5. RIKEN, Center for Brain Science (CBS), Saitama, Japan

6. The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, United States

Abstract

The ubiquitous presence of inhibitory interneurons in the thalamus of primates contrasts with the sparsity of interneurons reported in mice. Here, we identify a larger than expected complexity and distribution of interneurons across the mouse thalamus, where all thalamic interneurons can be traced back to two developmental programmes: one specified in the midbrain and the other in the forebrain. Interneurons migrate to functionally distinct thalamocortical nuclei depending on their origin: the abundant, midbrain-derived class populates the first and higher order sensory thalamus while the rarer, forebrain-generated class is restricted to some higher order associative regions. We also observe that markers for the midbrain-born class are abundantly expressed throughout the thalamus of the New World monkey marmoset. These data therefore reveal that, despite the broad variability in interneuron density across mammalian species, the blueprint of the ontogenetic organisation of thalamic interneurons of larger-brained mammals exists and can be studied in mice.

Funder

Biotechnology and Biological Sciences Research Council

Engineering and Physical Sciences Research Council

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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