Skip to main content
Top
Published in: Brain Structure and Function 3/2021

Open Access 01-04-2021 | Original Article

Quail-chick grafting experiments corroborate that Tbr1-positive eminential prethalamic neurons migrate along three streams into hypothalamus, subpallium and septocommissural areas

Authors: Antonia Alonso, Carmen María Trujillo, Luis Puelles

Published in: Brain Structure and Function | Issue 3/2021

Login to get access

Abstract

The prethalamic eminence (PThE), a diencephalic caudal neighbor of the telencephalon and alar hypothalamus, is frequently described in mammals and birds as a transient embryonic structure, undetectable in the adult brain. Based on descriptive developmental analysis of Tbr1 gene brain expression in chick embryos, we previously reported that three migratory cellular streams exit the PThE rostralward, targeting multiple sites in the hypothalamus, subpallium and septocommissural area, where eminential cells form distinct nuclei or disperse populations. These conclusions needed experimental corroboration. In this work, we used the homotopic quail-chick chimeric grafting procedure at stages HH10/HH11 to demonstrate by fate-mapping the three predicted tangential migration streams. Some chimeric brains were processed for Tbr1 in situ hybridization, for correlation with our previous approach. Evidence supporting all three postulated migration streams is presented. The results suggested a slight heterochrony among the juxtapeduncular (first), the peripeduncular (next), and the eminentio-septal (last) streams, each of which followed differential routes. A possible effect of such heterochrony on the differential selection of medial to lateral habenular hodologic targets by the migrated neurons is discussed.
Literature
go back to reference Alonso G, Szafarczyk A, Assenmacher I (1986) Radioautographic evidence that axons from the area of supraoptic nuclei in the rat project to extrahypothalamic brain regions. Neurosci Lett 66:251–256CrossRef Alonso G, Szafarczyk A, Assenmacher I (1986) Radioautographic evidence that axons from the area of supraoptic nuclei in the rat project to extrahypothalamic brain regions. Neurosci Lett 66:251–256CrossRef
go back to reference Alvarado-Mallart R-M (2000) Chapter 5 The chick/quail transplantation model to study central nervous system development. In: Progress in Brain Research. Elsevier, pp 67–98 Alvarado-Mallart R-M (2000) Chapter 5 The chick/quail transplantation model to study central nervous system development. In: Progress in Brain Research. Elsevier, pp 67–98
go back to reference Ferrán JL, Ayad A, Merchán P, Morales-Delgado N, Sánchez-Arrones L, Alonso A, Sandoval JE, Bardet SM, Corral-San-Miguel R, Sánchez-Guardado LO, Hidalgo-Sánchez M, Martínez-de-la-Torre M, Puelles L (2015a) Exploring brain genoarchitecture by single and double chromogenic in situ hybridization (ISH) and immunohistochemistry (IHC) on cryostat, paraffin, or floating sections. In: Hauptmann G (ed) In Situ Hybridization Methods, Neuromethods, vol 99. Springer Science + Business Media, New York, pp 83–107. https://doi.org/10.1007/978-1-4939-2303-8_5 Ferrán JL, Ayad A, Merchán P, Morales-Delgado N, Sánchez-Arrones L, Alonso A, Sandoval JE, Bardet SM, Corral-San-Miguel R, Sánchez-Guardado LO, Hidalgo-Sánchez M, Martínez-de-la-Torre M, Puelles L (2015a) Exploring brain genoarchitecture by single and double chromogenic in situ hybridization (ISH) and immunohistochemistry (IHC) on cryostat, paraffin, or floating sections. In: Hauptmann G (ed) In Situ Hybridization Methods, Neuromethods, vol 99. Springer Science + Business Media, New York, pp 83–107. https://​doi.​org/​10.​1007/​978-1-4939-2303-8_​5
go back to reference Guillén-Pérez M (1991) Estructura del epitálamo y complejo superior del tálamo dorsal en aves: estudio embriológico. Posibles homologías con mamíferos. Doctoral Thesis. Univ. de Murcia Guillén-Pérez M (1991) Estructura del epitálamo y complejo superior del tálamo dorsal en aves: estudio embriológico. Posibles homologías con mamíferos. Doctoral Thesis. Univ. de Murcia
go back to reference Hetzel W (1974) Die Ontogenese des Telencephalons bei Lcerta sicula (Rafinesque), mit besonderer Berücksichtigung der pallialen Entwicklung. Zool Beitr 20:361–458 Hetzel W (1974) Die Ontogenese des Telencephalons bei Lcerta sicula (Rafinesque), mit besonderer Berücksichtigung der pallialen Entwicklung. Zool Beitr 20:361–458
go back to reference Huilgol D, Udin S, Shimogori T, Saha B, Roy A, Aizawa S, Hevner RF, Meyer G, Ohshima T, Pleasure SJ, Zhao Y, Tole S (2013) Dual origins of the mammalian accessory olfactory bulb revealed by an evolutionarily conserved migratory stream. Nat Neurosci 16:157–165. https://doi.org/10.1038/nn.3297CrossRefPubMed Huilgol D, Udin S, Shimogori T, Saha B, Roy A, Aizawa S, Hevner RF, Meyer G, Ohshima T, Pleasure SJ, Zhao Y, Tole S (2013) Dual origins of the mammalian accessory olfactory bulb revealed by an evolutionarily conserved migratory stream. Nat Neurosci 16:157–165. https://​doi.​org/​10.​1038/​nn.​3297CrossRefPubMed
go back to reference Medina L, Abellán A (2012) Subpallial structures. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier, Amsterdan, pp 173–220CrossRef Medina L, Abellán A (2012) Subpallial structures. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier, Amsterdan, pp 173–220CrossRef
go back to reference Olivier C, Cobos I, Perez Villegas EM, Spassky N, Zalc B, Martinez S, Thomas JL (2001) Monofocal origin of telencephalic oligodendrocytes in the anterior entopeduncular area of the chick embryo. Development 128:1757–1769PubMed Olivier C, Cobos I, Perez Villegas EM, Spassky N, Zalc B, Martinez S, Thomas JL (2001) Monofocal origin of telencephalic oligodendrocytes in the anterior entopeduncular area of the chick embryo. Development 128:1757–1769PubMed
go back to reference Parent A (1979) Identification of the pallidal and peripallidal cells projecting to the habenula in monkey. Neurosci Lett 15:159–164CrossRef Parent A (1979) Identification of the pallidal and peripallidal cells projecting to the habenula in monkey. Neurosci Lett 15:159–164CrossRef
go back to reference Parent A (1986) Comparative neurobiology of the basal ganglia. Wiley & Sons, New York Parent A (1986) Comparative neurobiology of the basal ganglia. Wiley & Sons, New York
go back to reference Parent A, De Bellefeuille L (1982) Organization of efferent projections from the internal segment of globus pallidus in primate as revealed by fluorescence retrograde labeling method. Brain Res 245:201–213CrossRef Parent A, De Bellefeuille L (1982) Organization of efferent projections from the internal segment of globus pallidus in primate as revealed by fluorescence retrograde labeling method. Brain Res 245:201–213CrossRef
go back to reference Parent A, Gravel S, Boucher R (1981) The origin of forebrain afferents to the habenula in rat, cat and monkey. Brain Res Bull 6:23–38CrossRef Parent A, Gravel S, Boucher R (1981) The origin of forebrain afferents to the habenula in rat, cat and monkey. Brain Res Bull 6:23–38CrossRef
go back to reference Parent A, De Bellefeuille L, Mackey A (1984) Organization of primate internal pallidum as revealed by fluorescent retrograde tracing of its efferent projections. Adv Neurol 40:15–20PubMed Parent A, De Bellefeuille L, Mackey A (1984) Organization of primate internal pallidum as revealed by fluorescent retrograde tracing of its efferent projections. Adv Neurol 40:15–20PubMed
go back to reference Puelles L (2014) Development and evolution of the claustrum. In: Smythies JR, Edelstein LR, Ramachandran VS (eds) The Claustrum: Structural, Functional, and Clinical Neuroscience. Academic Press, San Diego, pp 119–176CrossRef Puelles L (2014) Development and evolution of the claustrum. In: Smythies JR, Edelstein LR, Ramachandran VS (eds) The Claustrum: Structural, Functional, and Clinical Neuroscience. Academic Press, San Diego, pp 119–176CrossRef
go back to reference Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martínez S (2007) The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies, 1st edn. Academic Press, Amsterdam Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martínez S (2007) The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies, 1st edn. Academic Press, Amsterdam
go back to reference Puelles L, Martinez-de-la-Torre M, Bardet S, Rubenstein JLR (2012a) Hypothalamus. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier, Amsterdan, pp 221–312CrossRef Puelles L, Martinez-de-la-Torre M, Bardet S, Rubenstein JLR (2012a) Hypothalamus. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier, Amsterdan, pp 221–312CrossRef
go back to reference Puelles L, Martinez-de-la-Torre M, Ferran J-L, Watson C (2012b) Diencephalon. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier, Amsterdam, pp 313–336CrossRef Puelles L, Martinez-de-la-Torre M, Ferran J-L, Watson C (2012b) Diencephalon. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Elsevier, Amsterdam, pp 313–336CrossRef
go back to reference Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martínez S (2019) The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies, 2nd edn. Academic Press, Amsterdam Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martínez S (2019) The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies, 2nd edn. Academic Press, Amsterdam
go back to reference Selleck MA, Bronner-Fraser M (1995) Origins of the avian neural crest: the role of neural plate-epidermal interactions. Development 121:525–538PubMed Selleck MA, Bronner-Fraser M (1995) Origins of the avian neural crest: the role of neural plate-epidermal interactions. Development 121:525–538PubMed
go back to reference Trujillo CM (1982) Ontogenesis of the thalamic nuclei in Gallotia galloti galloti: structural and ultrastructural study. Doctoral Thesis. University of La Laguna Trujillo CM (1982) Ontogenesis of the thalamic nuclei in Gallotia galloti galloti: structural and ultrastructural study. Doctoral Thesis. University of La Laguna
go back to reference Trujillo CM, Alvarado-Mallart RM (1991) Mapping of the presumptive diencephalic regions in chick/quail chimeras. XIV Annual Meeting of ENA. Cambridge. Eur J Neurosci Suppl 2 Trujillo CM, Alvarado-Mallart RM (1991) Mapping of the presumptive diencephalic regions in chick/quail chimeras. XIV Annual Meeting of ENA. Cambridge. Eur J Neurosci Suppl 2
go back to reference van der Kooy D, Carter DA (1981) The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat. Brain Res 211:15–36CrossRef van der Kooy D, Carter DA (1981) The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat. Brain Res 211:15–36CrossRef
Metadata
Title
Quail-chick grafting experiments corroborate that Tbr1-positive eminential prethalamic neurons migrate along three streams into hypothalamus, subpallium and septocommissural areas
Authors
Antonia Alonso
Carmen María Trujillo
Luis Puelles
Publication date
01-04-2021
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 3/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-020-02206-3

Other articles of this Issue 3/2021

Brain Structure and Function 3/2021 Go to the issue