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Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation

Understanding cortical microcircuits requires thorough measurement of physiological properties of synaptic connections formed within and between diverse subclasses of neurons. Towards this goal, we combined spatially precise optogenetic stimulation with multicellular recording to deeply characterize...

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Autores principales: Hage, Travis A, Bosma-Moody, Alice, Baker, Christopher A, Kratz, Megan B, Campagnola, Luke, Jarsky, Tim, Zeng, Hongkui, Murphy, Gabe J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8824465/
https://www.ncbi.nlm.nih.gov/pubmed/35060903
http://dx.doi.org/10.7554/eLife.71103
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author Hage, Travis A
Bosma-Moody, Alice
Baker, Christopher A
Kratz, Megan B
Campagnola, Luke
Jarsky, Tim
Zeng, Hongkui
Murphy, Gabe J
author_facet Hage, Travis A
Bosma-Moody, Alice
Baker, Christopher A
Kratz, Megan B
Campagnola, Luke
Jarsky, Tim
Zeng, Hongkui
Murphy, Gabe J
author_sort Hage, Travis A
collection PubMed
description Understanding cortical microcircuits requires thorough measurement of physiological properties of synaptic connections formed within and between diverse subclasses of neurons. Towards this goal, we combined spatially precise optogenetic stimulation with multicellular recording to deeply characterize intralaminar and translaminar monosynaptic connections to supragranular (L2/3) neurons in the mouse visual cortex. The reliability and specificity of multiphoton optogenetic stimulation were measured across multiple Cre lines, and measurements of connectivity were verified by comparison to paired recordings and targeted patching of optically identified presynaptic cells. With a focus on translaminar pathways, excitatory and inhibitory synaptic connections from genetically defined presynaptic populations were characterized by their relative abundance, spatial profiles, strength, and short-term dynamics. Consistent with the canonical cortical microcircuit, layer 4 excitatory neurons and interneurons within L2/3 represented the most common sources of input to L2/3 pyramidal cells. More surprisingly, we also observed strong excitatory connections from layer 5 intratelencephalic neurons and potent translaminar inhibition from multiple interneuron subclasses. The hybrid approach revealed convergence to and divergence from excitatory and inhibitory neurons within and across cortical layers. Divergent excitatory connections often spanned hundreds of microns of horizontal space. In contrast, divergent inhibitory connections were more frequently measured from postsynaptic targets near each other.
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spelling pubmed-88244652022-02-10 Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation Hage, Travis A Bosma-Moody, Alice Baker, Christopher A Kratz, Megan B Campagnola, Luke Jarsky, Tim Zeng, Hongkui Murphy, Gabe J eLife Neuroscience Understanding cortical microcircuits requires thorough measurement of physiological properties of synaptic connections formed within and between diverse subclasses of neurons. Towards this goal, we combined spatially precise optogenetic stimulation with multicellular recording to deeply characterize intralaminar and translaminar monosynaptic connections to supragranular (L2/3) neurons in the mouse visual cortex. The reliability and specificity of multiphoton optogenetic stimulation were measured across multiple Cre lines, and measurements of connectivity were verified by comparison to paired recordings and targeted patching of optically identified presynaptic cells. With a focus on translaminar pathways, excitatory and inhibitory synaptic connections from genetically defined presynaptic populations were characterized by their relative abundance, spatial profiles, strength, and short-term dynamics. Consistent with the canonical cortical microcircuit, layer 4 excitatory neurons and interneurons within L2/3 represented the most common sources of input to L2/3 pyramidal cells. More surprisingly, we also observed strong excitatory connections from layer 5 intratelencephalic neurons and potent translaminar inhibition from multiple interneuron subclasses. The hybrid approach revealed convergence to and divergence from excitatory and inhibitory neurons within and across cortical layers. Divergent excitatory connections often spanned hundreds of microns of horizontal space. In contrast, divergent inhibitory connections were more frequently measured from postsynaptic targets near each other. eLife Sciences Publications, Ltd 2022-01-21 /pmc/articles/PMC8824465/ /pubmed/35060903 http://dx.doi.org/10.7554/eLife.71103 Text en © 2022, Hage et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Hage, Travis A
Bosma-Moody, Alice
Baker, Christopher A
Kratz, Megan B
Campagnola, Luke
Jarsky, Tim
Zeng, Hongkui
Murphy, Gabe J
Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation
title Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation
title_full Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation
title_fullStr Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation
title_full_unstemmed Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation
title_short Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation
title_sort synaptic connectivity to l2/3 of primary visual cortex measured by two-photon optogenetic stimulation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8824465/
https://www.ncbi.nlm.nih.gov/pubmed/35060903
http://dx.doi.org/10.7554/eLife.71103
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