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A novel telencephalon-opto-hypothalamic morphogenetic domain produces most of the glutamatergic neurons of the medial extended amygdala

Lorena Morales, Beatriz Castro-Robles, View ORCID ProfileAntonio Abellán, View ORCID ProfileEster Desfilis, View ORCID ProfileLoreta Medina
doi: https://doi.org/10.1101/2020.07.17.207936
Lorena Morales
1Laboratory of Evolutionary and Developmental Neurobiology, Lleida’s Institute for Biomedical Research-Dr. Pifarré Foundation (IRBLleida), Catalonia, Spain
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Beatriz Castro-Robles
2Laboratory of Cerebrovascular, Neurodegenerative and Neuro-oncology Diseases, Research Unit, Complejo Hospitalario Universitario de Albacete, Castilla-La Mancha, Spain
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Antonio Abellán
1Laboratory of Evolutionary and Developmental Neurobiology, Lleida’s Institute for Biomedical Research-Dr. Pifarré Foundation (IRBLleida), Catalonia, Spain
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  • ORCID record for Antonio Abellán
Ester Desfilis
1Laboratory of Evolutionary and Developmental Neurobiology, Lleida’s Institute for Biomedical Research-Dr. Pifarré Foundation (IRBLleida), Catalonia, Spain
3Serra Húnter fellow
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  • For correspondence: loreta.medina@udl.cat desfilis@udl.cat
Loreta Medina
1Laboratory of Evolutionary and Developmental Neurobiology, Lleida’s Institute for Biomedical Research-Dr. Pifarré Foundation (IRBLleida), Catalonia, Spain
3Serra Húnter fellow
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  • For correspondence: loreta.medina@udl.cat desfilis@udl.cat
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Abstract

Deficits in social cognition and behavior are a hallmark of many psychiatric disorders. The medial extended amygdala, including the medial amygdala and the medial bed nucleus of the stria terminalis, is a key component of functional networks involved in sociality. However, this nuclear complex is highly heterogeneous and contains numerous GABAergic and glutamatergic neuron subpopulations. Deciphering the connections of different neurons is essential in order to understand how this structure regulates different aspects of sociality, and it is necessary to evaluate their differential implication in distinct mental disorders. Developmental studies in different vertebrates are offering new venues to understand neuronal diversity of the medial extended amygdala, and are helping to establish a relation between the embryonic origin and molecular signature of distinct neurons with the functional subcircuits in which they are engaged. These studies have provided many details on the distinct GABAergic neurons of the medial extended amygdala, but information on the glutamatergic neurons is still scarce. Using an Otp-eGFP transgenic mouse and multiple fluorescent labeling, we show that most glutamatergic neurons of the medial extended amygdala originate in a novel telencephalo-opto-hypothalamic embryonic domain (TOH), located at the transition between telencephalon and hypothalamus, which produces Otp-lineage neurons expressing the telencephalic marker Foxg1 but not Nkx2.1 during development. These glutamatergic cells include a subpopulation of projection neurons of the medial amygdala, which activation has been previously shown to promote autistic-like behavior. Our data open new venues for studying the implication of this neuron subtype in neurodevelopmental disorders producing social deficits.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations

    AAv
    ventral anterior amygdala
    ac
    anterior commissure
    AH
    anterior hypothalamus
    BC
    amygdalar basolateral complex
    BMa
    basomedial amygdala, anterior subnucleus
    BSTM
    medial bed nucleus of the stria terminalis
    BSTMa
    BSTM, anterior division
    BSTMh
    BSTM, hypothalamic subdivision/ hypothalamic subdivision of BSTM
    BSTMp
    BSTM, posterior division
    BSTL
    lateral bed nucleus of the stria terminalis
    Ce
    central nucleus of the amygdala (or simply central amygdala)
    Cer
    cerebellum
    CPu
    caudate-putamen complex
    DM
    dorsomedial hypothalamic nucleus
    EM
    median eminence
    ESO
    episupraoptic nucleus
    f
    fornix
    GP
    globus pallidus
    HF
    hippocampal formation
    Hya
    alar hypothalamus
    Hyb
    basal hypothalamus
    LH
    lateral hypothalamus
    LH
    basal LH
    LOT
    nucleus of the lateral olfactory tract
    LPO
    lateral preoptic area
    lv
    lateral ventricle
    m
    mantle
    Ma
    mammillary nuclei
    Me
    medial nucleus of the amygdala (or simply, medial amygdala)
    MeA
    anterior subnucleus of Me
    MeP
    posterior subnucleus of Me
    MePD
    dorsal subnucleus of MeP
    MePV
    ventral subnucleus of MeP
    MePVm
    medial branch of MePV
    MePVl
    lateral branch of MePV
    MGEvc
    medial glaglionic eminence, ventrocaudal subdivision
    NH
    neurohypophysis
    OB
    olfactory bulb
    oc
    optic chiasm
    op
    optic pedicle
    ot
    optic tract
    P
    pallium
    Pad
    paraventricular nucleus, dorsal subdivision
    Pav
    paraventricular nucleus, ventral subdivision
    Pt
    pretectum
    PHy
    peduncular hypothalamus
    POPe
    periventricular part of the preoptic area
    POs
    subpallial preoptic area
    POv
    ventral preoptic area
    PTh
    prethalamus
    PThE
    prethalamic eminence
    PVN
    paraventricular nucleus, principal subdivision
    Se
    septum
    SEA
    sublenticular extended amygdala
    SO
    supraoptic nucleus, principal subdivision
    SOt
    supraoptic nucleus, terminal subdivision
    SOtu
    of the supraoptic nucleus, tuberal subdivision
    Sp
    subpallium
    SC
    superior colliculus
    SCN
    suprachiasmatic nucleus
    SPa
    subparaventricular region
    SPV
    supraopto-paraventricular hypothalamic domain (classical definition)
    SPVc
    supraopto-paraventricular hypothalamic domain, core part
    svz
    subventricular zone
    Tel
    telencephalon
    Th
    thalamus
    THy
    terminal hypothalamus
    TOH
    telencephalo-opto-hypothalamic embryonic domain
    VMH
    ventromedial hypothalamic nucleus
    vz
    ventricular zone
    3v
    third ventricle
    4v
    fourth ventricle
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    A novel telencephalon-opto-hypothalamic morphogenetic domain produces most of the glutamatergic neurons of the medial extended amygdala
    Lorena Morales, Beatriz Castro-Robles, Antonio Abellán, Ester Desfilis, Loreta Medina
    bioRxiv 2020.07.17.207936; doi: https://doi.org/10.1101/2020.07.17.207936
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    A novel telencephalon-opto-hypothalamic morphogenetic domain produces most of the glutamatergic neurons of the medial extended amygdala
    Lorena Morales, Beatriz Castro-Robles, Antonio Abellán, Ester Desfilis, Loreta Medina
    bioRxiv 2020.07.17.207936; doi: https://doi.org/10.1101/2020.07.17.207936

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