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Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse
The immature retina generates spontaneous waves of spiking activity that sweep across the ganglion cell layer during a limited period of development before the onset of visual experience. The spatiotemporal patterns encoded in the waves are believed to be instructive for the wiring of functional con...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley & Sons Ltd
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3979611/ https://www.ncbi.nlm.nih.gov/pubmed/24366261 http://dx.doi.org/10.1113/jphysiol.2013.262840 |
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author | Maccione, Alessandro Hennig, Matthias H Gandolfo, Mauro Muthmann, Oliver van Coppenhagen, James Eglen, Stephen J Berdondini, Luca Sernagor, Evelyne |
author_facet | Maccione, Alessandro Hennig, Matthias H Gandolfo, Mauro Muthmann, Oliver van Coppenhagen, James Eglen, Stephen J Berdondini, Luca Sernagor, Evelyne |
author_sort | Maccione, Alessandro |
collection | PubMed |
description | The immature retina generates spontaneous waves of spiking activity that sweep across the ganglion cell layer during a limited period of development before the onset of visual experience. The spatiotemporal patterns encoded in the waves are believed to be instructive for the wiring of functional connections throughout the visual system. However, the ontogeny of retinal waves is still poorly documented as a result of the relatively low resolution of conventional recording techniques. Here, we characterize the spatiotemporal features of mouse retinal waves from birth until eye opening in unprecedented detail using a large-scale, dense, 4096-channel multielectrode array that allowed us to record from the entire neonatal retina at near cellular resolution. We found that early cholinergic waves propagate with random trajectories over large areas with low ganglion cell recruitment. They become slower, smaller and denser when GABA(A) signalling matures, as occurs beyond postnatal day (P) 7. Glutamatergic influences dominate from P10, coinciding with profound changes in activity dynamics. At this time, waves cease to be random and begin to show repetitive trajectories confined to a few localized hotspots. These hotspots gradually tile the retina with time, and disappear after eye opening. Our observations demonstrate that retinal waves undergo major spatiotemporal changes during ontogeny. Our results support the hypotheses that cholinergic waves guide the refinement of retinal targets and that glutamatergic waves may also support the wiring of retinal receptive fields. |
format | Online Article Text |
id | pubmed-3979611 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | John Wiley & Sons Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-39796112014-05-22 Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse Maccione, Alessandro Hennig, Matthias H Gandolfo, Mauro Muthmann, Oliver van Coppenhagen, James Eglen, Stephen J Berdondini, Luca Sernagor, Evelyne J Physiol Neuroscience: Development/Plasticity/Repair The immature retina generates spontaneous waves of spiking activity that sweep across the ganglion cell layer during a limited period of development before the onset of visual experience. The spatiotemporal patterns encoded in the waves are believed to be instructive for the wiring of functional connections throughout the visual system. However, the ontogeny of retinal waves is still poorly documented as a result of the relatively low resolution of conventional recording techniques. Here, we characterize the spatiotemporal features of mouse retinal waves from birth until eye opening in unprecedented detail using a large-scale, dense, 4096-channel multielectrode array that allowed us to record from the entire neonatal retina at near cellular resolution. We found that early cholinergic waves propagate with random trajectories over large areas with low ganglion cell recruitment. They become slower, smaller and denser when GABA(A) signalling matures, as occurs beyond postnatal day (P) 7. Glutamatergic influences dominate from P10, coinciding with profound changes in activity dynamics. At this time, waves cease to be random and begin to show repetitive trajectories confined to a few localized hotspots. These hotspots gradually tile the retina with time, and disappear after eye opening. Our observations demonstrate that retinal waves undergo major spatiotemporal changes during ontogeny. Our results support the hypotheses that cholinergic waves guide the refinement of retinal targets and that glutamatergic waves may also support the wiring of retinal receptive fields. John Wiley & Sons Ltd 2014-04-01 2014-01-31 /pmc/articles/PMC3979611/ /pubmed/24366261 http://dx.doi.org/10.1113/jphysiol.2013.262840 Text en © 2014 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society. http://creativecommons.org/licenses/by/3.0/ This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Neuroscience: Development/Plasticity/Repair Maccione, Alessandro Hennig, Matthias H Gandolfo, Mauro Muthmann, Oliver van Coppenhagen, James Eglen, Stephen J Berdondini, Luca Sernagor, Evelyne Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse |
title | Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse |
title_full | Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse |
title_fullStr | Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse |
title_full_unstemmed | Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse |
title_short | Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse |
title_sort | following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse |
topic | Neuroscience: Development/Plasticity/Repair |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3979611/ https://www.ncbi.nlm.nih.gov/pubmed/24366261 http://dx.doi.org/10.1113/jphysiol.2013.262840 |
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