Pattern formation in the striatum: Neurons with early projections to the substantia nigra survive the cell death period

Gordon Fishell, Derek Van Der Kooy

Research output: Contribution to journalArticle

Abstract

During the early postnatal period the striatum undergoes significant cell death. The specificity and regulation of this regressive event may be particularly interesting in the light of recent findings demonstrating that a developmentally organized compartmental architecture exists in the striatum. The striatum can be divided into two complementary and phenotypically distinct compartments, the patches and the matrix. In the adult, these two striatal compartments can be distinguished on the basis of their anatomy and a series of compartment‐specific biochemical and hodological markers. We have previously demonstrated that the neurons within the patch and matrix compartments become postmitotic and make connections with the substantia nigra at distinct and sequential developmental times. The majority of patch neurons become postmitotic between embryonic days 12 and 15 and make a striatonigral connection prenatally. In contrast, a majority of matrix neurons become postmitotic between embryonic days 17 and 20 and do not form an efferent connection to the substantia nigra until the first postnatal week. Here we investigated whether either neuronal birthdate or time of making an efferent projection correlates with a neuron's probability of surviving the cell death period. We found that both the patch and matrix compartments undergo their entire cell death period by the end of the first postnatal week. During this period approximately 30% of striatal neurons are subject to cell death, regardless of striatal compartment. Neuronal counts within the striatal patch compartment suggest that both early born neurons (embryonic day 13) and early projecting neurons (to the substantia nigra) are preferentially spared. However, their considerable overlap (i.e., most early born neurons also have a nigral projection) prevents assessment of which feature is critical for survival. In contrast, there are small, but mostly separate, populations of early born and early projecting neurons within the matrix compartment. Quantitative analysis of these two distinct populations suggests that while early projection neurons within the matrix are spared, the early born matrix neurons lacking an early nigral projection undergo significant cell death. This proposal is further supported by the observation that the percentage of early born neurons in both the patch and matrix compartments that also have an early nigral projection increases from postnatal day 2 to 17. This finding suggests that among the early born striatal neurons in both compartments, those that do not project to the nigra selectively die during the cell death period. Together these results support the hypothesis that completion of an early projection to the substantia nigra gives neurons an advantage for surviving the cell death period.

Original languageEnglish (US)
Pages (from-to)33-42
Number of pages10
JournalJournal of Comparative Neurology
Volume312
Issue number1
DOIs
StatePublished - Jan 1 1991

Fingerprint

Substantia Nigra
Cell Death
Neurons
Corpus Striatum
Population
Anatomy
Biomarkers

Keywords

  • neuronal birthdate
  • retrograde labeling
  • striatal matrix compartment
  • striatal patch compartment
  • trophic support

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Pattern formation in the striatum : Neurons with early projections to the substantia nigra survive the cell death period. / Fishell, Gordon; Van Der Kooy, Derek.

In: Journal of Comparative Neurology, Vol. 312, No. 1, 01.01.1991, p. 33-42.

Research output: Contribution to journalArticle

@article{b0d3c3d14b134f7cbecc3a54d7cc738c,
title = "Pattern formation in the striatum: Neurons with early projections to the substantia nigra survive the cell death period",
abstract = "During the early postnatal period the striatum undergoes significant cell death. The specificity and regulation of this regressive event may be particularly interesting in the light of recent findings demonstrating that a developmentally organized compartmental architecture exists in the striatum. The striatum can be divided into two complementary and phenotypically distinct compartments, the patches and the matrix. In the adult, these two striatal compartments can be distinguished on the basis of their anatomy and a series of compartment‐specific biochemical and hodological markers. We have previously demonstrated that the neurons within the patch and matrix compartments become postmitotic and make connections with the substantia nigra at distinct and sequential developmental times. The majority of patch neurons become postmitotic between embryonic days 12 and 15 and make a striatonigral connection prenatally. In contrast, a majority of matrix neurons become postmitotic between embryonic days 17 and 20 and do not form an efferent connection to the substantia nigra until the first postnatal week. Here we investigated whether either neuronal birthdate or time of making an efferent projection correlates with a neuron's probability of surviving the cell death period. We found that both the patch and matrix compartments undergo their entire cell death period by the end of the first postnatal week. During this period approximately 30{\%} of striatal neurons are subject to cell death, regardless of striatal compartment. Neuronal counts within the striatal patch compartment suggest that both early born neurons (embryonic day 13) and early projecting neurons (to the substantia nigra) are preferentially spared. However, their considerable overlap (i.e., most early born neurons also have a nigral projection) prevents assessment of which feature is critical for survival. In contrast, there are small, but mostly separate, populations of early born and early projecting neurons within the matrix compartment. Quantitative analysis of these two distinct populations suggests that while early projection neurons within the matrix are spared, the early born matrix neurons lacking an early nigral projection undergo significant cell death. This proposal is further supported by the observation that the percentage of early born neurons in both the patch and matrix compartments that also have an early nigral projection increases from postnatal day 2 to 17. This finding suggests that among the early born striatal neurons in both compartments, those that do not project to the nigra selectively die during the cell death period. Together these results support the hypothesis that completion of an early projection to the substantia nigra gives neurons an advantage for surviving the cell death period.",
keywords = "neuronal birthdate, retrograde labeling, striatal matrix compartment, striatal patch compartment, trophic support",
author = "Gordon Fishell and {Van Der Kooy}, Derek",
year = "1991",
month = "1",
day = "1",
doi = "10.1002/cne.903120104",
language = "English (US)",
volume = "312",
pages = "33--42",
journal = "Journal of Comparative Neurology",
issn = "0021-9967",
publisher = "Wiley-Liss Inc.",
number = "1",

}

TY - JOUR

T1 - Pattern formation in the striatum

T2 - Neurons with early projections to the substantia nigra survive the cell death period

AU - Fishell, Gordon

AU - Van Der Kooy, Derek

PY - 1991/1/1

Y1 - 1991/1/1

N2 - During the early postnatal period the striatum undergoes significant cell death. The specificity and regulation of this regressive event may be particularly interesting in the light of recent findings demonstrating that a developmentally organized compartmental architecture exists in the striatum. The striatum can be divided into two complementary and phenotypically distinct compartments, the patches and the matrix. In the adult, these two striatal compartments can be distinguished on the basis of their anatomy and a series of compartment‐specific biochemical and hodological markers. We have previously demonstrated that the neurons within the patch and matrix compartments become postmitotic and make connections with the substantia nigra at distinct and sequential developmental times. The majority of patch neurons become postmitotic between embryonic days 12 and 15 and make a striatonigral connection prenatally. In contrast, a majority of matrix neurons become postmitotic between embryonic days 17 and 20 and do not form an efferent connection to the substantia nigra until the first postnatal week. Here we investigated whether either neuronal birthdate or time of making an efferent projection correlates with a neuron's probability of surviving the cell death period. We found that both the patch and matrix compartments undergo their entire cell death period by the end of the first postnatal week. During this period approximately 30% of striatal neurons are subject to cell death, regardless of striatal compartment. Neuronal counts within the striatal patch compartment suggest that both early born neurons (embryonic day 13) and early projecting neurons (to the substantia nigra) are preferentially spared. However, their considerable overlap (i.e., most early born neurons also have a nigral projection) prevents assessment of which feature is critical for survival. In contrast, there are small, but mostly separate, populations of early born and early projecting neurons within the matrix compartment. Quantitative analysis of these two distinct populations suggests that while early projection neurons within the matrix are spared, the early born matrix neurons lacking an early nigral projection undergo significant cell death. This proposal is further supported by the observation that the percentage of early born neurons in both the patch and matrix compartments that also have an early nigral projection increases from postnatal day 2 to 17. This finding suggests that among the early born striatal neurons in both compartments, those that do not project to the nigra selectively die during the cell death period. Together these results support the hypothesis that completion of an early projection to the substantia nigra gives neurons an advantage for surviving the cell death period.

AB - During the early postnatal period the striatum undergoes significant cell death. The specificity and regulation of this regressive event may be particularly interesting in the light of recent findings demonstrating that a developmentally organized compartmental architecture exists in the striatum. The striatum can be divided into two complementary and phenotypically distinct compartments, the patches and the matrix. In the adult, these two striatal compartments can be distinguished on the basis of their anatomy and a series of compartment‐specific biochemical and hodological markers. We have previously demonstrated that the neurons within the patch and matrix compartments become postmitotic and make connections with the substantia nigra at distinct and sequential developmental times. The majority of patch neurons become postmitotic between embryonic days 12 and 15 and make a striatonigral connection prenatally. In contrast, a majority of matrix neurons become postmitotic between embryonic days 17 and 20 and do not form an efferent connection to the substantia nigra until the first postnatal week. Here we investigated whether either neuronal birthdate or time of making an efferent projection correlates with a neuron's probability of surviving the cell death period. We found that both the patch and matrix compartments undergo their entire cell death period by the end of the first postnatal week. During this period approximately 30% of striatal neurons are subject to cell death, regardless of striatal compartment. Neuronal counts within the striatal patch compartment suggest that both early born neurons (embryonic day 13) and early projecting neurons (to the substantia nigra) are preferentially spared. However, their considerable overlap (i.e., most early born neurons also have a nigral projection) prevents assessment of which feature is critical for survival. In contrast, there are small, but mostly separate, populations of early born and early projecting neurons within the matrix compartment. Quantitative analysis of these two distinct populations suggests that while early projection neurons within the matrix are spared, the early born matrix neurons lacking an early nigral projection undergo significant cell death. This proposal is further supported by the observation that the percentage of early born neurons in both the patch and matrix compartments that also have an early nigral projection increases from postnatal day 2 to 17. This finding suggests that among the early born striatal neurons in both compartments, those that do not project to the nigra selectively die during the cell death period. Together these results support the hypothesis that completion of an early projection to the substantia nigra gives neurons an advantage for surviving the cell death period.

KW - neuronal birthdate

KW - retrograde labeling

KW - striatal matrix compartment

KW - striatal patch compartment

KW - trophic support

UR - http://www.scopus.com/inward/record.url?scp=0025946443&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0025946443&partnerID=8YFLogxK

U2 - 10.1002/cne.903120104

DO - 10.1002/cne.903120104

M3 - Article

C2 - 1660493

AN - SCOPUS:0025946443

VL - 312

SP - 33

EP - 42

JO - Journal of Comparative Neurology

JF - Journal of Comparative Neurology

SN - 0021-9967

IS - 1

ER -