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

doi:10.1016/S0896-6273(03)00437-9

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

Developmental Neurobiology

Research output: Contribution to journal › Article › peer-review

138 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 language	English
Pages (from-to)	423-438
Number of pages	16
Journal	Neuron
Volume	39
Issue number	3
DOIs	https://doi.org/10.1016/S0896-6273(03)00437-9
Publication status	Published - 31 Jul 2003

Keywords

Cell Movement
Animals
Molecular Sequence Data
Animals, Genetically Modified
Central Nervous System
Zebrafish
Prosencephalon
Functional Laterality

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Concha, M. L., Russell, C., Regan, J. C., Tawk, M., Sidi, S., Gilmour, D. T., Kapsimali, M., Sumoy, L., Goldstone, K., Amaya, E., Kimelman, D., Nicolson, T., Gründer, S., Gomperts, M., Clarke, J. D. W., & 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

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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.",

keywords = "Cell Movement, Animals, Molecular Sequence Data, Animals, Genetically Modified, Central Nervous System, Zebrafish, Prosencephalon, Functional Laterality",

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}",

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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

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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

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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.

KW - Cell Movement

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KW - Molecular Sequence Data

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KW - Central Nervous System

KW - Zebrafish

KW - Prosencephalon

KW - Functional Laterality

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

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VL - 39

SP - 423

EP - 438

JO - Neuron

JF - Neuron

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ER -

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

Abstract

Keywords

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