Adult axolotls can regenerate original neuronal diversity in response to brain injury

The axolotl can regenerate multiple organs, including the brain. It remains, however, unclear whether neuronal diversity, intricate tissue architecture, and axonal connectivity can be regenerated; yet, this is critical for recovery of function and a central aim of cell replacement strategies in the...

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Main Authors: Ryoji Amamoto, Violeta Gisselle Lopez Huerta, Emi Takahashi, Guangping Dai, Aaron K Grant, Zhanyan Fu, Paola Arlotta
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/13998
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author Ryoji Amamoto
Violeta Gisselle Lopez Huerta
Emi Takahashi
Guangping Dai
Aaron K Grant
Zhanyan Fu
Paola Arlotta
author_facet Ryoji Amamoto
Violeta Gisselle Lopez Huerta
Emi Takahashi
Guangping Dai
Aaron K Grant
Zhanyan Fu
Paola Arlotta
author_sort Ryoji Amamoto
collection DOAJ
description The axolotl can regenerate multiple organs, including the brain. It remains, however, unclear whether neuronal diversity, intricate tissue architecture, and axonal connectivity can be regenerated; yet, this is critical for recovery of function and a central aim of cell replacement strategies in the mammalian central nervous system. Here, we demonstrate that, upon mechanical injury to the adult pallium, axolotls can regenerate several of the populations of neurons present before injury. Notably, regenerated neurons acquire functional electrophysiological traits and respond appropriately to afferent inputs. Despite the ability to regenerate specific, molecularly-defined neuronal subtypes, we also uncovered previously unappreciated limitations by showing that newborn neurons organize within altered tissue architecture and fail to re-establish the long-distance axonal tracts and circuit physiology present before injury. The data provide a direct demonstration that diverse, electrophysiologically functional neurons can be regenerated in axolotls, but challenge prior assumptions of functional brain repair in regenerative species.
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spelling doaj.art-0ac70644369a4eb89161a44248bf7cfb2022-12-22T03:52:41ZengeLife Sciences Publications LtdeLife2050-084X2016-05-01510.7554/eLife.13998Adult axolotls can regenerate original neuronal diversity in response to brain injuryRyoji Amamoto0Violeta Gisselle Lopez Huerta1Emi Takahashi2Guangping Dai3Aaron K Grant4Zhanyan Fu5Paola Arlotta6https://orcid.org/0000-0003-2184-2277Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, United StatesStanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, United StatesDivision of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United StatesDepartment of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, United StatesStanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, United StatesDepartment of Stem Cell and Regenerative Biology, Harvard University, Cambridge, United States; Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, United StatesThe axolotl can regenerate multiple organs, including the brain. It remains, however, unclear whether neuronal diversity, intricate tissue architecture, and axonal connectivity can be regenerated; yet, this is critical for recovery of function and a central aim of cell replacement strategies in the mammalian central nervous system. Here, we demonstrate that, upon mechanical injury to the adult pallium, axolotls can regenerate several of the populations of neurons present before injury. Notably, regenerated neurons acquire functional electrophysiological traits and respond appropriately to afferent inputs. Despite the ability to regenerate specific, molecularly-defined neuronal subtypes, we also uncovered previously unappreciated limitations by showing that newborn neurons organize within altered tissue architecture and fail to re-establish the long-distance axonal tracts and circuit physiology present before injury. The data provide a direct demonstration that diverse, electrophysiologically functional neurons can be regenerated in axolotls, but challenge prior assumptions of functional brain repair in regenerative species.https://elifesciences.org/articles/13998Axolotlbrain regenerationneuronal diversity
spellingShingle Ryoji Amamoto
Violeta Gisselle Lopez Huerta
Emi Takahashi
Guangping Dai
Aaron K Grant
Zhanyan Fu
Paola Arlotta
Adult axolotls can regenerate original neuronal diversity in response to brain injury
eLife
Axolotl
brain regeneration
neuronal diversity
title Adult axolotls can regenerate original neuronal diversity in response to brain injury
title_full Adult axolotls can regenerate original neuronal diversity in response to brain injury
title_fullStr Adult axolotls can regenerate original neuronal diversity in response to brain injury
title_full_unstemmed Adult axolotls can regenerate original neuronal diversity in response to brain injury
title_short Adult axolotls can regenerate original neuronal diversity in response to brain injury
title_sort adult axolotls can regenerate original neuronal diversity in response to brain injury
topic Axolotl
brain regeneration
neuronal diversity
url https://elifesciences.org/articles/13998
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