Four alpha ganglion cell types in mouse retina: Function, structure, and molecular signatures

The retina communicates with the brain using ≥30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian retina one finds so-called "alpha" ganglion cells (αRGCs), identified by their large cell bodies, stout axons, wide and mono-stratified...

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Vydáno v:	PloS one Ročník 12; číslo 7; s. e0180091
Hlavní autoři:	Krieger, Brenna, Qiao, Mu, Rousso, David L., Sanes, Joshua R., Meister, Markus
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States Public Library of Science 28.07.2017 Public Library of Science (PLoS)
Témata:	Action potential Action Potentials - physiology Analysis Animals Asymmetry Axons Axons - metabolism BASIC (programming language) Biology and Life Sciences Brain Cellular biology Channels Dendrites - metabolism Diagnosis Electrophysiology Female Ganglion cysts Gene expression Genetic aspects Genetic engineering Health aspects Integrases - metabolism Kinetics Laboratory animals Light effects Male Mammals Medicine and Health Sciences Mice Molecular structure Morphology Neurofilaments Neurons Neurosciences Physiology Polarity Potassium Channels, Voltage-Gated - metabolism Receptive field Retina Retina - cytology Retinal ganglion cells Retinal Ganglion Cells - metabolism Signaling Social Sciences Structure-function relationships Transgenic mice Transient response Visual aspects Visual Pathways - physiology Visual signals United States > US Massachusetts California
ISSN:	1932-6203, 1932-6203
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Abstract	The retina communicates with the brain using ≥30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian retina one finds so-called "alpha" ganglion cells (αRGCs), identified by their large cell bodies, stout axons, wide and mono-stratified dendritic fields, and high levels of neurofilament protein. In the mouse, three αRGC types have been described based on responses to light steps: On-sustained, Off-sustained, and Off-transient. Here we employed a transgenic mouse line that labels αRGCs in the live retina, allowing systematic targeted recordings. We characterize the three known types and identify a fourth, with On-transient responses. All four αRGC types share basic aspects of visual signaling, including a large receptive field center, a weak antagonistic surround, and absence of any direction selectivity. They also share a distinctive waveform of the action potential, faster than that of other RGC types. Morphologically, they differ in the level of dendritic stratification within the IPL, which accounts for their response properties. Molecularly, each type has a distinct signature. A comparison across mammals suggests a common theme, in which four large-bodied ganglion cell types split the visual signal into four channels arranged symmetrically with respect to polarity and kinetics.
AbstractList	The retina communicates with the brain using [greater than or equal to]30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian retina one finds so-called "alpha" ganglion cells ([alpha]RGCs), identified by their large cell bodies, stout axons, wide and mono-stratified dendritic fields, and high levels of neurofilament protein. In the mouse, three [alpha]RGC types have been described based on responses to light steps: On-sustained, Off-sustained, and Off-transient. Here we employed a transgenic mouse line that labels [alpha]RGCs in the live retina, allowing systematic targeted recordings. We characterize the three known types and identify a fourth, with On-transient responses. All four [alpha]RGC types share basic aspects of visual signaling, including a large receptive field center, a weak antagonistic surround, and absence of any direction selectivity. They also share a distinctive waveform of the action potential, faster than that of other RGC types. Morphologically, they differ in the level of dendritic stratification within the IPL, which accounts for their response properties. Molecularly, each type has a distinct signature. A comparison across mammals suggests a common theme, in which four large-bodied ganglion cell types split the visual signal into four channels arranged symmetrically with respect to polarity and kinetics. The retina communicates with the brain using ≥30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian retina one finds so-called "alpha" ganglion cells (αRGCs), identified by their large cell bodies, stout axons, wide and mono-stratified dendritic fields, and high levels of neurofilament protein. In the mouse, three αRGC types have been described based on responses to light steps: On-sustained, Off-sustained, and Off-transient. Here we employed a transgenic mouse line that labels αRGCs in the live retina, allowing systematic targeted recordings. We characterize the three known types and identify a fourth, with On-transient responses. All four αRGC types share basic aspects of visual signaling, including a large receptive field center, a weak antagonistic surround, and absence of any direction selectivity. They also share a distinctive waveform of the action potential, faster than that of other RGC types. Morphologically, they differ in the level of dendritic stratification within the IPL, which accounts for their response properties. Molecularly, each type has a distinct signature. A comparison across mammals suggests a common theme, in which four large-bodied ganglion cell types split the visual signal into four channels arranged symmetrically with respect to polarity and kinetics. The retina communicates with the brain using ≥30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian retina one finds so-called "alpha" ganglion cells (αRGCs), identified by their large cell bodies, stout axons, wide and mono-stratified dendritic fields, and high levels of neurofilament protein. In the mouse, three αRGC types have been described based on responses to light steps: On-sustained, Off-sustained, and Off-transient. Here we employed a transgenic mouse line that labels αRGCs in the live retina, allowing systematic targeted recordings. We characterize the three known types and identify a fourth, with On-transient responses. All four αRGC types share basic aspects of visual signaling, including a large receptive field center, a weak antagonistic surround, and absence of any direction selectivity. They also share a distinctive waveform of the action potential, faster than that of other RGC types. Morphologically, they differ in the level of dendritic stratification within the IPL, which accounts for their response properties. Molecularly, each type has a distinct signature. A comparison across mammals suggests a common theme, in which four large-bodied ganglion cell types split the visual signal into four channels arranged symmetrically with respect to polarity and kinetics.The retina communicates with the brain using ≥30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian retina one finds so-called "alpha" ganglion cells (αRGCs), identified by their large cell bodies, stout axons, wide and mono-stratified dendritic fields, and high levels of neurofilament protein. In the mouse, three αRGC types have been described based on responses to light steps: On-sustained, Off-sustained, and Off-transient. Here we employed a transgenic mouse line that labels αRGCs in the live retina, allowing systematic targeted recordings. We characterize the three known types and identify a fourth, with On-transient responses. All four αRGC types share basic aspects of visual signaling, including a large receptive field center, a weak antagonistic surround, and absence of any direction selectivity. They also share a distinctive waveform of the action potential, faster than that of other RGC types. Morphologically, they differ in the level of dendritic stratification within the IPL, which accounts for their response properties. Molecularly, each type has a distinct signature. A comparison across mammals suggests a common theme, in which four large-bodied ganglion cell types split the visual signal into four channels arranged symmetrically with respect to polarity and kinetics.
Audience	Academic
Author	Meister, Markus Krieger, Brenna Qiao, Mu Rousso, David L. Sanes, Joshua R.
AuthorAffiliation	2 Center for Brain Science and Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts, United States of America Dalhousie University, CANADA 1 Harvard Biophysics Program, Harvard Medical School, Boston, Massachusetts, United States of America 3 Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California, United States of America
AuthorAffiliation_xml	– name: 1 Harvard Biophysics Program, Harvard Medical School, Boston, Massachusetts, United States of America – name: 2 Center for Brain Science and Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts, United States of America – name: Dalhousie University, CANADA – name: 3 Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California, United States of America
Author_xml	– sequence: 1 givenname: Brenna surname: Krieger fullname: Krieger, Brenna – sequence: 2 givenname: Mu surname: Qiao fullname: Qiao, Mu – sequence: 3 givenname: David L. surname: Rousso fullname: Rousso, David L. – sequence: 4 givenname: Joshua R. surname: Sanes fullname: Sanes, Joshua R. – sequence: 5 givenname: Markus orcidid: 0000-0003-2136-6506 surname: Meister fullname: Meister, Markus
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28753612$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	COPYRIGHT 2017 Public Library of Science 2017 Krieger et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2017 Krieger et al 2017 Krieger et al
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceptualization: BK MQ JS MM.Data curation: BK MQ DR MM.Formal analysis: BK MQ DR JS MM.Funding acquisition: DR JS MM.Investigation: BK MQ DR.Methodology: BK DR JS MM.Project administration: JS MM.Software: BK DR MM.Supervision: JS MM.Validation: JS MM.Visualization: BK MM.Writing – original draft: BK MM.Writing – review & editing: BK MQ DR JS MM. Competing Interests: The authors have declared that no competing interests exist.
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Snippet	The retina communicates with the brain using ≥30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian... The retina communicates with the brain using [greater than or equal to]30 parallel channels, each carried by axons of distinct types of retinal ganglion cells....
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SubjectTerms	Action potential Action Potentials - physiology Analysis Animals Asymmetry Axons Axons - metabolism BASIC (programming language) Biology and Life Sciences Brain Cellular biology Channels Dendrites - metabolism Diagnosis Electrophysiology Female Ganglion cysts Gene expression Genetic aspects Genetic engineering Health aspects Integrases - metabolism Kinetics Laboratory animals Light effects Male Mammals Medicine and Health Sciences Mice Molecular structure Morphology Neurofilaments Neurons Neurosciences Physiology Polarity Potassium Channels, Voltage-Gated - metabolism Receptive field Retina Retina - cytology Retinal ganglion cells Retinal Ganglion Cells - metabolism Signaling Social Sciences Structure-function relationships Transgenic mice Transient response Visual aspects Visual Pathways - physiology Visual signals
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Title	Four alpha ganglion cell types in mouse retina: Function, structure, and molecular signatures
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