Evolutionary and developmental contributions for understanding the organization of the basal ganglia

Herein we take advantage of the evolutionary developmental biology approach in order to improve our understanding of both the functional organization and the evolution of the basal ganglia, with a particular focus on the globus pallidus. Therefore, we review data on the expression of developmental r...

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Autores: Medina Hernández, Loreta Mª, Abellán Ródenas, Antonio, Vicario Andrade, Alba, Desfilis, Ester
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2014
País:España
Institución:Universitat de Lleida (UdL)
Repositorio:Repositori Obert UdL
OAI Identifier:oai:repositori.udl.cat:10459.1/66159
Acceso en línea:https://doi.org/10.1159/000357832
http://hdl.handle.net/10459.1/66159
Access Level:acceso abierto
Palabra clave:Forebrain evolution
Developmental regulatory genes
Enkephalin
Globus pallidus
Pallidostriatal projections
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spelling Evolutionary and developmental contributions for understanding the organization of the basal gangliaMedina Hernández, Loreta MªAbellán Ródenas, AntonioVicario Andrade, AlbaDesfilis, EsterForebrain evolutionDevelopmental regulatory genesEnkephalinGlobus pallidusPallidostriatal projectionsHerein we take advantage of the evolutionary developmental biology approach in order to improve our understanding of both the functional organization and the evolution of the basal ganglia, with a particular focus on the globus pallidus. Therefore, we review data on the expression of developmental regulatory genes (that play key roles in patterning, regional specification and/or morphogenesis), gene function and fate mapping available in different vertebrate species, which are useful to (a) understand the embryonic origin and basic features of each neuron subtype of the basal ganglia (including neurotransmitter/neuropeptide expression and connectivity patterns); (b) identify the same (homologous) subpopulations in different species and the degree of variation or conservation throughout phylogeny, and (c) identify possible mechanisms that may explain the evolution of the basal ganglia. These data show that the globus pallidus of rodents contains two major subpopulations of GABAergic projection neurons: (1) neurons containing parvalbumin and neurotensin-related hexapetide (LANT6), with descending projections to the subthalamus and substantia nigra, which originate from progenitors expressing Nkx2.1, primarily located in the pallidal embryonic domain (medial ganglionic eminence), and (2) neurons containing preproenkephalin (and possibly calbindin), with ascending projections to the striatum, which appear to originate from progenitors expressing Islet1 in the striatal embryonic domain (lateral ganglionic eminence). Based on data on Nkx2.1, Islet1, LANT6 and proenkephalin, it appears that both cell types are also present in the globus pallidus/dorsal pallidum of chicken, frog and lungfish. In chicken, the globus pallidus also contains neurons expressing substance P (SP), perhaps originating in the striatal embryonic domain. In ray-finned and cartilaginous fishes, the pallidum contains at least the Nkx2.1 lineage cell population (likely representing the neurons containing LANT6). Based on the presence of neurons containing enkephalin or SP, it is possible that the pallidum of these animals also includes the Islet1 lineage cell subpopulation, and both neuron subtypes were likely present in the pallidum of the first jawed vertebrates. In contrast, lampreys (jawless fishes) appear to lack the pallidal embryonic domain and the Nkx2.1 lineage cell population that mainly characterize the pallidum in jawed vertebrates. In the absence of data in other jawless fishes, the ancestral condition in vertebrates remains to be elucidated. Perhaps, a major event in telencephalic evolution was the novel expression of Nkx2.1 in the subpallium, which has been related to Hedgehog expression and changes in the regulatory region of Nkx2.1.This study was supported by a grant from the Spanish Ministry of Economy and Competitivity, and Fondo Europeo de Desarrollo Regional (FEDER): grant No. BFU2012-33029.Karger2014info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://doi.org/10.1159/000357832http://hdl.handle.net/10459.1/66159reponame:Repositori Obert UdL instname:Universitat de Lleida (UdL)Inglésinfo:eu-repo/grantAgreement/MICINN//BFU2012-33029Reproducció del document publicat a: https://doi.org/10.1159/000357832Brain Behavior and Evolution, 2014, vol. 83, núm. 2, p. 112-125cc-by-nc (c) S. Karger AG, Basel, 2014info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc/3.0/oai:repositori.udl.cat:10459.1/661592026-06-24T12:42:17Z
dc.title.none.fl_str_mv Evolutionary and developmental contributions for understanding the organization of the basal ganglia
title Evolutionary and developmental contributions for understanding the organization of the basal ganglia
spellingShingle Evolutionary and developmental contributions for understanding the organization of the basal ganglia
Medina Hernández, Loreta Mª
Forebrain evolution
Developmental regulatory genes
Enkephalin
Globus pallidus
Pallidostriatal projections
title_short Evolutionary and developmental contributions for understanding the organization of the basal ganglia
title_full Evolutionary and developmental contributions for understanding the organization of the basal ganglia
title_fullStr Evolutionary and developmental contributions for understanding the organization of the basal ganglia
title_full_unstemmed Evolutionary and developmental contributions for understanding the organization of the basal ganglia
title_sort Evolutionary and developmental contributions for understanding the organization of the basal ganglia
dc.creator.none.fl_str_mv Medina Hernández, Loreta Mª
Abellán Ródenas, Antonio
Vicario Andrade, Alba
Desfilis, Ester
author Medina Hernández, Loreta Mª
author_facet Medina Hernández, Loreta Mª
Abellán Ródenas, Antonio
Vicario Andrade, Alba
Desfilis, Ester
author_role author
author2 Abellán Ródenas, Antonio
Vicario Andrade, Alba
Desfilis, Ester
author2_role author
author
author
dc.subject.none.fl_str_mv Forebrain evolution
Developmental regulatory genes
Enkephalin
Globus pallidus
Pallidostriatal projections
topic Forebrain evolution
Developmental regulatory genes
Enkephalin
Globus pallidus
Pallidostriatal projections
description Herein we take advantage of the evolutionary developmental biology approach in order to improve our understanding of both the functional organization and the evolution of the basal ganglia, with a particular focus on the globus pallidus. Therefore, we review data on the expression of developmental regulatory genes (that play key roles in patterning, regional specification and/or morphogenesis), gene function and fate mapping available in different vertebrate species, which are useful to (a) understand the embryonic origin and basic features of each neuron subtype of the basal ganglia (including neurotransmitter/neuropeptide expression and connectivity patterns); (b) identify the same (homologous) subpopulations in different species and the degree of variation or conservation throughout phylogeny, and (c) identify possible mechanisms that may explain the evolution of the basal ganglia. These data show that the globus pallidus of rodents contains two major subpopulations of GABAergic projection neurons: (1) neurons containing parvalbumin and neurotensin-related hexapetide (LANT6), with descending projections to the subthalamus and substantia nigra, which originate from progenitors expressing Nkx2.1, primarily located in the pallidal embryonic domain (medial ganglionic eminence), and (2) neurons containing preproenkephalin (and possibly calbindin), with ascending projections to the striatum, which appear to originate from progenitors expressing Islet1 in the striatal embryonic domain (lateral ganglionic eminence). Based on data on Nkx2.1, Islet1, LANT6 and proenkephalin, it appears that both cell types are also present in the globus pallidus/dorsal pallidum of chicken, frog and lungfish. In chicken, the globus pallidus also contains neurons expressing substance P (SP), perhaps originating in the striatal embryonic domain. In ray-finned and cartilaginous fishes, the pallidum contains at least the Nkx2.1 lineage cell population (likely representing the neurons containing LANT6). Based on the presence of neurons containing enkephalin or SP, it is possible that the pallidum of these animals also includes the Islet1 lineage cell subpopulation, and both neuron subtypes were likely present in the pallidum of the first jawed vertebrates. In contrast, lampreys (jawless fishes) appear to lack the pallidal embryonic domain and the Nkx2.1 lineage cell population that mainly characterize the pallidum in jawed vertebrates. In the absence of data in other jawless fishes, the ancestral condition in vertebrates remains to be elucidated. Perhaps, a major event in telencephalic evolution was the novel expression of Nkx2.1 in the subpallium, which has been related to Hedgehog expression and changes in the regulatory region of Nkx2.1.
publishDate 2014
dc.date.none.fl_str_mv 2014
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://doi.org/10.1159/000357832
http://hdl.handle.net/10459.1/66159
url https://doi.org/10.1159/000357832
http://hdl.handle.net/10459.1/66159
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv info:eu-repo/grantAgreement/MICINN//BFU2012-33029
Reproducció del document publicat a: https://doi.org/10.1159/000357832
Brain Behavior and Evolution, 2014, vol. 83, núm. 2, p. 112-125
dc.rights.none.fl_str_mv cc-by-nc (c) S. Karger AG, Basel, 2014
info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc/3.0/
rights_invalid_str_mv cc-by-nc (c) S. Karger AG, Basel, 2014
https://creativecommons.org/licenses/by-nc/3.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Karger
publisher.none.fl_str_mv Karger
dc.source.none.fl_str_mv reponame:Repositori Obert UdL
instname:Universitat de Lleida (UdL)
instname_str Universitat de Lleida (UdL)
reponame_str Repositori Obert UdL
collection Repositori Obert UdL
repository.name.fl_str_mv
repository.mail.fl_str_mv
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