Dual midbrain and forebrain origins of thalamic inhibitory interneurons

TY - JOUR

T1 - Dual midbrain and forebrain origins of thalamic inhibitory interneurons

AU - Jager, Polona

AU - Moore, Gerald

AU - Calpin, Padraic

AU - Durmishi, Xhuljana

AU - Salgarella, Irene

AU - Menage, Lucy

AU - Kita, Yoshiaki

AU - Wang, Yan

AU - Kim, Dong Won

AU - Blackshaw, Seth

AU - Schultz, Simon R

AU - Brickley, Stephen

AU - Shimogori, Tomomi

AU - Delogu, Alessio

N1 - Funding Information: We thank the Wohl Cellular Imaging Centre, King?s College London for support with imaging and image analysis software. We are grateful to Beatriz Rico, Monica Moissidis, and Patricia Hernandez at King?s College London for the Nkx2.1Cre; Rosa26lsl-GFP and the Lhx6Cre; Rosa26lsl-GFP samples. We are grateful to the anonymous peer reviewers for their constructive and specific comments. This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/ L020068/1 and BB/R007020/1 to AD and BB/R007659/1 to SB. Two-photon tomography was developed with Engineering and Physical Sciences Research Council (EPSRC) grant EP/J021199/1 to SRS. Publisher Copyright: © Jager et al. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/2

Y1 - 2021/2

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85101974643&partnerID=8YFLogxK

U2 - 10.7554/eLife.59272

DO - 10.7554/eLife.59272

M3 - Article

C2 - 33522480

SN - 2050-084X

VL - 10

SP - 1

EP - 29

JO - eLife

JF - eLife

M1 - e59272

ER -