Tangential migration of corridor guidepost neurons contributes to anxiety circuits

Andrea Tinterri; Marie Deck; Maryama Keita; Caroline Mailhes; Anna Noren Rubin; Nicoletta Kessaris; Ludmilla Lokmane; Franck Bielle; Sonia Garel

doi:10.1002/cne.24330

Tangential migration of corridor guidepost neurons contributes to anxiety circuits

J Comp Neurol. 2018 Feb 15;526(3):397-411. doi: 10.1002/cne.24330. Epub 2017 Oct 11.

Authors

Andrea Tinterri^{1

2

3

4}, Marie Deck^{1

2}, Maryama Keita^{1

2}, Caroline Mailhes^{1

5}, Anna Noren Rubin⁶, Nicoletta Kessaris⁶, Ludmilla Lokmane^{1

2}, Franck Bielle^{1

2

7}, Sonia Garel^{1

2

4}

Affiliations

¹ IBENS, Département de Biologie, École normale supérieure, CNRS, Inserm, PSL Research University, Paris, France.
² Brain Development and Plasticity Team.
³ Boehringer Ingelheim Fonds, Foundation for Basic Research in Medicine, Mainz, Germany.
⁴ Ecole de Neurosciences de Paris-Ile de France, Paris, France.
⁵ Acute Transgenesis Facility.
⁶ University College of London, Wolfson Institute for Biomedical Research, Department of Cell and Developmental Biology, London, United Kingdom.
⁷ AP-HP, Hôpitaux Universitaires Pitié-Salpêtrière Charles Foix, Service de Neuropathologie, Paris, France.

PMID: 28921616
DOI: 10.1002/cne.24330

Abstract

In mammals, thalamic axons are guided internally toward their neocortical target by corridor (Co) neurons that act as axonal guideposts. The existence of Co-like neurons in non-mammalian species, in which thalamic axons do not grow internally, raised the possibility that Co cells might have an ancestral role. Here, we investigated the contribution of corridor (Co) cells to mature brain circuits using a combination of genetic fate-mapping and assays in mice. We unexpectedly found that Co neurons contribute to striatal-like projection neurons in the central extended amygdala. In particular, Co-like neurons participate in specific nuclei of the bed nucleus of the stria terminalis, which plays essential roles in anxiety circuits. Our study shows that Co neurons possess an evolutionary conserved role in anxiety circuits independently from an acquired guidepost function. It furthermore highlights that neurons can have multiple sequential functions during brain wiring and supports a general role of tangential migration in the building of subpallial circuits.

Keywords: BNST; Islet1; RRID:IMSR_JAX:024242; RRID:MGI:4840402; RRID:MMRRC_000230-UNC; central extended amygdale; corridor neurons; forebrain development; guidepost cells; tangential migration.

MeSH terms

Afferent Pathways / physiology*
Animals
Animals, Newborn
Axon Guidance / genetics*
Cell Movement / physiology*
Cholera Toxin / metabolism
Deoxyuridine / analogs & derivatives
Deoxyuridine / metabolism
Embryo, Mammalian
Female
Gene Expression Regulation, Developmental / physiology*
Green Fluorescent Proteins / genetics
Green Fluorescent Proteins / metabolism
LIM-Homeodomain Proteins / genetics
LIM-Homeodomain Proteins / metabolism
Male
Mice
Mice, Inbred C57BL
Mice, Transgenic
Pontine Tegmentum* / cytology
Pontine Tegmentum* / embryology
Pontine Tegmentum* / growth & development
Pregnancy
Receptors, Dopamine D2 / genetics
Receptors, Dopamine D2 / metabolism
Thalamus* / cytology
Thalamus* / embryology
Thalamus* / growth & development
Thyroid Nuclear Factor 1 / metabolism
Trans-Activators / genetics
Trans-Activators / metabolism
Transcription Factors / genetics
Transcription Factors / metabolism

Substances

DRD2 protein, mouse
Ebf1 protein, mouse
LIM-Homeodomain Proteins
Nkx2-1 protein, mouse
Receptors, Dopamine D2
Thyroid Nuclear Factor 1
Trans-Activators
Transcription Factors
enhanced green fluorescent protein
insulin gene enhancer binding protein Isl-1
Green Fluorescent Proteins
Cholera Toxin
5-ethynyl-1-(3-hydroxy-4-(hydroxymethyl)cyclopentyl)-2,4(1H,3H)-pyrimidinedione
Deoxyuridine