Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum

The mature striatum is divided into a labyrinthine system of striosomes embedded in a surrounding matrix compartment. We pulse-labeled striosomal cells (S cells) and matrix cells (M cells) in cats with [superscript 3]H-thymidine and followed their distributions during fetal and postnatal development...

Full description

Bibliographic Details
Main Authors: Newman, Helen, Liu, Fu-Chin, Graybiel, Ann M.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:en_US
Published: Wiley Blackwell 2016
Online Access:http://hdl.handle.net/1721.1/102427
https://orcid.org/0000-0002-4326-7720
_version_ 1826193308957802496
author Newman, Helen
Liu, Fu-Chin
Graybiel, Ann M.
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Newman, Helen
Liu, Fu-Chin
Graybiel, Ann M.
author_sort Newman, Helen
collection MIT
description The mature striatum is divided into a labyrinthine system of striosomes embedded in a surrounding matrix compartment. We pulse-labeled striosomal cells (S cells) and matrix cells (M cells) in cats with [superscript 3]H-thymidine and followed their distributions during fetal and postnatal development. We identified three maturational phases in S-cell distributions. The early phase (sampled at embryonic day [E]27–E35 following E24-E28 [superscript 3]H-thymidine) was characterized by a transient medial accumulation of synchronously generated S cells within the caudate nucleus adjoining the ganglionic eminence, potentially a waiting compartment. Band-like arrangements of synchronously generated S cells then formed beyond this medial band. During the second phase (sampled at E38–E45), the loosely banded S-cell distributions were transformed into clustered arrangements typical of developing striosomes. In the third phase (sampled from E52 into the postnatal period), these developed into the typical mature striosomal architecture. At adulthood, gentle mediolateral birthdate-gradients in S cells were still evident, but M cells, produced over mid to late prenatal ages, became broadly distributed, without apparent gradients or banding arrangements. These findings suggest that the maturational histories of the striosomal and matrix neurons are influenced by their generation times and local environments, and that future S cells have transient, nonstriosomal distributions prior to their aggregation into striosomal clusters, including a putative waiting compartment. Further, the eventual patterning of the striosomal compartment reflects outside-in, band-like gradient patterns of settling of synchronously generated S cells, patterns that could be related both to neural processing in the mature striatum and to patterns of vulnerability of striatal neurons.
first_indexed 2024-09-23T09:36:56Z
format Article
id mit-1721.1/102427
institution Massachusetts Institute of Technology
language en_US
last_indexed 2024-09-23T09:36:56Z
publishDate 2016
publisher Wiley Blackwell
record_format dspace
spelling mit-1721.1/1024272022-09-26T12:41:58Z Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum Newman, Helen Liu, Fu-Chin Graybiel, Ann M. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Graybiel, Ann M. The mature striatum is divided into a labyrinthine system of striosomes embedded in a surrounding matrix compartment. We pulse-labeled striosomal cells (S cells) and matrix cells (M cells) in cats with [superscript 3]H-thymidine and followed their distributions during fetal and postnatal development. We identified three maturational phases in S-cell distributions. The early phase (sampled at embryonic day [E]27–E35 following E24-E28 [superscript 3]H-thymidine) was characterized by a transient medial accumulation of synchronously generated S cells within the caudate nucleus adjoining the ganglionic eminence, potentially a waiting compartment. Band-like arrangements of synchronously generated S cells then formed beyond this medial band. During the second phase (sampled at E38–E45), the loosely banded S-cell distributions were transformed into clustered arrangements typical of developing striosomes. In the third phase (sampled from E52 into the postnatal period), these developed into the typical mature striosomal architecture. At adulthood, gentle mediolateral birthdate-gradients in S cells were still evident, but M cells, produced over mid to late prenatal ages, became broadly distributed, without apparent gradients or banding arrangements. These findings suggest that the maturational histories of the striosomal and matrix neurons are influenced by their generation times and local environments, and that future S cells have transient, nonstriosomal distributions prior to their aggregation into striosomal clusters, including a putative waiting compartment. Further, the eventual patterning of the striosomal compartment reflects outside-in, band-like gradient patterns of settling of synchronously generated S cells, patterns that could be related both to neural processing in the mature striatum and to patterns of vulnerability of striatal neurons. Wills Foundation Eunice Kennedy Shriver National Institute of Child Health and Human Development (U.S.) (Grant R37 HD028341) Hereditary Disease Foundation (U.S.) Cure Huntington’s Disease Initiative, Inc. (Grant A-5552) 2016-05-09T14:34:13Z 2016-05-09T14:34:13Z 2015-01 2014-12 Article http://purl.org/eprint/type/JournalArticle 00219967 1096-9861 http://hdl.handle.net/1721.1/102427 Newman, Helen, Fu-Chin Liu, and Ann M. Graybiel. “Dynamic Ordering of Early Generated Striatal Cells Destined to Form the Striosomal Compartment of the Striatum.” J. Comp. Neurol. 523, no. 6 (January 30, 2015): 943–962. https://orcid.org/0000-0002-4326-7720 en_US http://dx.doi.org/10.1002/cne.23725 Journal of Comparative Neurology Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf Wiley Blackwell PMC
spellingShingle Newman, Helen
Liu, Fu-Chin
Graybiel, Ann M.
Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum
title Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum
title_full Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum
title_fullStr Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum
title_full_unstemmed Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum
title_short Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum
title_sort dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum
url http://hdl.handle.net/1721.1/102427
https://orcid.org/0000-0002-4326-7720
work_keys_str_mv AT newmanhelen dynamicorderingofearlygeneratedstriatalcellsdestinedtoformthestriosomalcompartmentofthestriatum
AT liufuchin dynamicorderingofearlygeneratedstriatalcellsdestinedtoformthestriosomalcompartmentofthestriatum
AT graybielannm dynamicorderingofearlygeneratedstriatalcellsdestinedtoformthestriosomalcompartmentofthestriatum