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Embryonic and postnatal development of mouse olfactory tubercle.

Abstract

The olfactory tubercle (OT) is located in the ventral-medial region of the brain where it receives primary input from olfactory bulb (OB) projection neurons and processes olfactory behaviors related to motivation, hedonics of smell and sexual encounters. The OT is part of the dopamine reward system that shares characteristics with the striatum. Together with the nucleus accumbens, the OT has been referred to as the "ventral striatum". However, despite its functional importance little is known about the embryonic development of the OT and the phenotypic properties of the OT cells. Here, using thymidine analogs, we establish that mouse OT neurogenesis occurs predominantly between E11-E15 in a lateral-to-medial gradient. Then, using a piggyBac multicolor technique we characterized the migratory route of OT neuroblasts from their embryonic point of origin. Following neurogenesis in the ventral lateral ganglionic eminence (vLGE), neuroblasts destined for the OT followed a dorsal-ventral pathway we named "ventral migratory course" (VMC). Upon reaching the nascent OT, neurons established a prototypical laminar distribution that was determined, in part, by the progenitor cell of origin. A phenotypic analysis of OT neuroblasts using a single-color piggyBac technique, showed that OT shared the molecular specification of striatal neurons. In addition to primary afferent input from the OB, the OT also receives a robust dopaminergic input from ventral tegmentum (Ikemoto, 2007). We used tyrosine hydroxylase (TH) expression as a proxy for dopaminergic innervation and showed that TH onset occurs at E13 and progressively increased until postnatal stages following an 'inside-out' pattern. Postnatally, we established the myelination in the OT occurring between P7 and P14, as shown with CNPase staining, and we characterized the cellular phenotypes populating the OT by immunohistochemistry. Collectively, this work provides the first detailed analysis of the developmental and maturation processes occurring in mouse OT, and demonstrates the striatal nature of the OT as part of the ventral striatum (vST).

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  • Authors+Show Affiliations

    ,

    Department of Neuroscience, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA; Department of Neurosurgery, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA.

    ,

    Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA.

    ,

    Department of Neuroscience, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA; Department of Neurosurgery, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA.

    ,

    Department of Neuroscience, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA; Department of Neurosurgery, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA; The Interdepartmental Neuroscience Graduate Program, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA.

    Department of Neuroscience, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA; Department of Neurosurgery, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA; The Interdepartmental Neuroscience Graduate Program, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA. Electronic address: charles.greer@yale.edu.

    Source

    Pub Type(s)

    Journal Article

    Language

    eng

    PubMed ID

    31200100

    Citation

    Martin-Lopez, Eduardo, et al. "Embryonic and Postnatal Development of Mouse Olfactory Tubercle." Molecular and Cellular Neurosciences, vol. 98, 2019, pp. 82-96.
    Martin-Lopez E, Xu C, Liberia T, et al. Embryonic and postnatal development of mouse olfactory tubercle. Mol Cell Neurosci. 2019;98:82-96.
    Martin-Lopez, E., Xu, C., Liberia, T., Meller, S. J., & Greer, C. A. (2019). Embryonic and postnatal development of mouse olfactory tubercle. Molecular and Cellular Neurosciences, 98, pp. 82-96. doi:10.1016/j.mcn.2019.06.002.
    Martin-Lopez E, et al. Embryonic and Postnatal Development of Mouse Olfactory Tubercle. Mol Cell Neurosci. 2019;98:82-96. PubMed PMID: 31200100.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Embryonic and postnatal development of mouse olfactory tubercle. AU - Martin-Lopez,Eduardo, AU - Xu,Christine, AU - Liberia,Teresa, AU - Meller,Sarah J, AU - Greer,Charles A, Y1 - 2019/06/11/ PY - 2018/12/20/received PY - 2019/05/09/revised PY - 2019/06/10/accepted PY - 2019/6/15/pubmed PY - 2019/6/15/medline PY - 2019/6/15/entrez KW - Development KW - Dopaminergic innervation KW - Myelination KW - Neurogenesis KW - Olfactory tubercle KW - Striatum SP - 82 EP - 96 JF - Molecular and cellular neurosciences JO - Mol. Cell. Neurosci. VL - 98 N2 - The olfactory tubercle (OT) is located in the ventral-medial region of the brain where it receives primary input from olfactory bulb (OB) projection neurons and processes olfactory behaviors related to motivation, hedonics of smell and sexual encounters. The OT is part of the dopamine reward system that shares characteristics with the striatum. Together with the nucleus accumbens, the OT has been referred to as the "ventral striatum". However, despite its functional importance little is known about the embryonic development of the OT and the phenotypic properties of the OT cells. Here, using thymidine analogs, we establish that mouse OT neurogenesis occurs predominantly between E11-E15 in a lateral-to-medial gradient. Then, using a piggyBac multicolor technique we characterized the migratory route of OT neuroblasts from their embryonic point of origin. Following neurogenesis in the ventral lateral ganglionic eminence (vLGE), neuroblasts destined for the OT followed a dorsal-ventral pathway we named "ventral migratory course" (VMC). Upon reaching the nascent OT, neurons established a prototypical laminar distribution that was determined, in part, by the progenitor cell of origin. A phenotypic analysis of OT neuroblasts using a single-color piggyBac technique, showed that OT shared the molecular specification of striatal neurons. In addition to primary afferent input from the OB, the OT also receives a robust dopaminergic input from ventral tegmentum (Ikemoto, 2007). We used tyrosine hydroxylase (TH) expression as a proxy for dopaminergic innervation and showed that TH onset occurs at E13 and progressively increased until postnatal stages following an 'inside-out' pattern. Postnatally, we established the myelination in the OT occurring between P7 and P14, as shown with CNPase staining, and we characterized the cellular phenotypes populating the OT by immunohistochemistry. Collectively, this work provides the first detailed analysis of the developmental and maturation processes occurring in mouse OT, and demonstrates the striatal nature of the OT as part of the ventral striatum (vST). SN - 1095-9327 UR - https://www.unboundmedicine.com/medline/citation/31200100/Embryonic_and_postnatal_development_of_mouse_olfactory_tubercle L2 - https://linkinghub.elsevier.com/retrieve/pii/S1044-7431(18)30418-4 DB - PRIME DP - Unbound Medicine ER -