Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality

Miguel L. Concha, Claire Russell, Jennifer C. Regan, Marcel Tawk, Samuel Sidi, Darren T. Gilmour, Marika Kapsimali, Lauro Sumoy, Kim Goldstone, Enrique Amaya, David Kimelman, Teresa Nicolson, Stefan Gründer, Miranda Gomperts, Jonathan D W Clarke, Stephen W. Wilson

Research output: Contribution to journalArticle

117 Citations (Scopus)

Abstract

The mechanisms that establish behavioral, cognitive, and neuroanatomical asymmetries are poorly understood. In this study, we analyze the events that regulate development of asymmetric nuclei in the dorsal forebrain. The unilateral parapineal organ has a bilateral origin, and some parapineal precursors migrate across the midline to form this left-sided nucleus. The parapineal subsequently innervates the left habenula, which derives from ventral epithalamic cells adjacent to the parapineal precursors. Ablation of cells in the left ventral epithalamus can reverse laterality in wild-type embryos and impose the direction of CNS asymmetry in embryos in which laterality is usually randomized. Unilateral modulation of Nodal activity by Lefty1 can also impose the direction of CNS laterality in embryos with bilateral expression of Nodal pathway genes. From these data, we propose that laterality is determined by a competitive interaction between the left and right epithalamus and that Nodal signaling biases the outcome of this competition.

Original languageEnglish (US)
Pages (from-to)423-438
Number of pages16
JournalNeuron
Volume39
Issue number3
DOIs
StatePublished - Jul 31 2003
Externally publishedYes

Fingerprint

Epithalamus
Prosencephalon
Embryonic Structures
Habenula
Genes
Direction compound

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Concha, M. L., Russell, C., Regan, J. C., Tawk, M., Sidi, S., Gilmour, D. T., ... Wilson, S. W. (2003). Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron, 39(3), 423-438. https://doi.org/10.1016/S0896-6273(03)00437-9

Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. / Concha, Miguel L.; Russell, Claire; Regan, Jennifer C.; Tawk, Marcel; Sidi, Samuel; Gilmour, Darren T.; Kapsimali, Marika; Sumoy, Lauro; Goldstone, Kim; Amaya, Enrique; Kimelman, David; Nicolson, Teresa; Gründer, Stefan; Gomperts, Miranda; Clarke, Jonathan D W; Wilson, Stephen W.

In: Neuron, Vol. 39, No. 3, 31.07.2003, p. 423-438.

Research output: Contribution to journalArticle

Concha, ML, Russell, C, Regan, JC, Tawk, M, Sidi, S, Gilmour, DT, Kapsimali, M, Sumoy, L, Goldstone, K, Amaya, E, Kimelman, D, Nicolson, T, Gründer, S, Gomperts, M, Clarke, JDW & Wilson, SW 2003, 'Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality', Neuron, vol. 39, no. 3, pp. 423-438. https://doi.org/10.1016/S0896-6273(03)00437-9
Concha ML, Russell C, Regan JC, Tawk M, Sidi S, Gilmour DT et al. Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron. 2003 Jul 31;39(3):423-438. https://doi.org/10.1016/S0896-6273(03)00437-9
Concha, Miguel L. ; Russell, Claire ; Regan, Jennifer C. ; Tawk, Marcel ; Sidi, Samuel ; Gilmour, Darren T. ; Kapsimali, Marika ; Sumoy, Lauro ; Goldstone, Kim ; Amaya, Enrique ; Kimelman, David ; Nicolson, Teresa ; Gründer, Stefan ; Gomperts, Miranda ; Clarke, Jonathan D W ; Wilson, Stephen W. / Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. In: Neuron. 2003 ; Vol. 39, No. 3. pp. 423-438.
@article{cfa56aed40264040aa11340d88e5995b,
title = "Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality",
abstract = "The mechanisms that establish behavioral, cognitive, and neuroanatomical asymmetries are poorly understood. In this study, we analyze the events that regulate development of asymmetric nuclei in the dorsal forebrain. The unilateral parapineal organ has a bilateral origin, and some parapineal precursors migrate across the midline to form this left-sided nucleus. The parapineal subsequently innervates the left habenula, which derives from ventral epithalamic cells adjacent to the parapineal precursors. Ablation of cells in the left ventral epithalamus can reverse laterality in wild-type embryos and impose the direction of CNS asymmetry in embryos in which laterality is usually randomized. Unilateral modulation of Nodal activity by Lefty1 can also impose the direction of CNS laterality in embryos with bilateral expression of Nodal pathway genes. From these data, we propose that laterality is determined by a competitive interaction between the left and right epithalamus and that Nodal signaling biases the outcome of this competition.",
author = "Concha, {Miguel L.} and Claire Russell and Regan, {Jennifer C.} and Marcel Tawk and Samuel Sidi and Gilmour, {Darren T.} and Marika Kapsimali and Lauro Sumoy and Kim Goldstone and Enrique Amaya and David Kimelman and Teresa Nicolson and Stefan Gr{\"u}nder and Miranda Gomperts and Clarke, {Jonathan D W} and Wilson, {Stephen W.}",
year = "2003",
month = "7",
day = "31",
doi = "10.1016/S0896-6273(03)00437-9",
language = "English (US)",
volume = "39",
pages = "423--438",
journal = "Neuron",
issn = "0896-6273",
publisher = "Cell Press",
number = "3",

}

TY - JOUR

T1 - Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality

AU - Concha, Miguel L.

AU - Russell, Claire

AU - Regan, Jennifer C.

AU - Tawk, Marcel

AU - Sidi, Samuel

AU - Gilmour, Darren T.

AU - Kapsimali, Marika

AU - Sumoy, Lauro

AU - Goldstone, Kim

AU - Amaya, Enrique

AU - Kimelman, David

AU - Nicolson, Teresa

AU - Gründer, Stefan

AU - Gomperts, Miranda

AU - Clarke, Jonathan D W

AU - Wilson, Stephen W.

PY - 2003/7/31

Y1 - 2003/7/31

N2 - The mechanisms that establish behavioral, cognitive, and neuroanatomical asymmetries are poorly understood. In this study, we analyze the events that regulate development of asymmetric nuclei in the dorsal forebrain. The unilateral parapineal organ has a bilateral origin, and some parapineal precursors migrate across the midline to form this left-sided nucleus. The parapineal subsequently innervates the left habenula, which derives from ventral epithalamic cells adjacent to the parapineal precursors. Ablation of cells in the left ventral epithalamus can reverse laterality in wild-type embryos and impose the direction of CNS asymmetry in embryos in which laterality is usually randomized. Unilateral modulation of Nodal activity by Lefty1 can also impose the direction of CNS laterality in embryos with bilateral expression of Nodal pathway genes. From these data, we propose that laterality is determined by a competitive interaction between the left and right epithalamus and that Nodal signaling biases the outcome of this competition.

AB - The mechanisms that establish behavioral, cognitive, and neuroanatomical asymmetries are poorly understood. In this study, we analyze the events that regulate development of asymmetric nuclei in the dorsal forebrain. The unilateral parapineal organ has a bilateral origin, and some parapineal precursors migrate across the midline to form this left-sided nucleus. The parapineal subsequently innervates the left habenula, which derives from ventral epithalamic cells adjacent to the parapineal precursors. Ablation of cells in the left ventral epithalamus can reverse laterality in wild-type embryos and impose the direction of CNS asymmetry in embryos in which laterality is usually randomized. Unilateral modulation of Nodal activity by Lefty1 can also impose the direction of CNS laterality in embryos with bilateral expression of Nodal pathway genes. From these data, we propose that laterality is determined by a competitive interaction between the left and right epithalamus and that Nodal signaling biases the outcome of this competition.

UR - http://www.scopus.com/inward/record.url?scp=0042196074&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0042196074&partnerID=8YFLogxK

U2 - 10.1016/S0896-6273(03)00437-9

DO - 10.1016/S0896-6273(03)00437-9

M3 - Article

C2 - 12895418

AN - SCOPUS:0042196074

VL - 39

SP - 423

EP - 438

JO - Neuron

JF - Neuron

SN - 0896-6273

IS - 3

ER -