Three-dimensional multi-site random access photostimulation (3D-MAP)

Optical control of neural ensemble activity is crucial for understanding brain function and disease, yet no technology can achieve optogenetic control of very large numbers of neurons at an extremely fast rate over a large volume. State-of-the-art multiphoton holographic optogenetics requires high-p...

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Main Authors: Yi Xue, Laura Waller, Hillel Adesnik, Nicolas Pégard
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/73266
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author Yi Xue
Laura Waller
Hillel Adesnik
Nicolas Pégard
author_facet Yi Xue
Laura Waller
Hillel Adesnik
Nicolas Pégard
author_sort Yi Xue
collection DOAJ
description Optical control of neural ensemble activity is crucial for understanding brain function and disease, yet no technology can achieve optogenetic control of very large numbers of neurons at an extremely fast rate over a large volume. State-of-the-art multiphoton holographic optogenetics requires high-power illumination that only addresses relatively small populations of neurons in parallel. Conversely, one-photon holographic techniques can stimulate more neurons with two to three orders lower power, but with limited resolution or addressable volume. Perhaps most problematically, two-photon holographic optogenetic systems are extremely expensive and sophisticated which has precluded their broader adoption in the neuroscience community. To address this technical gap, we introduce a new one-photon light sculpting technique, three-dimensional multi-site random access photostimulation (3D-MAP), that overcomes these limitations by modulating light dynamically, both in the spatial and in the angular domain at multi-kHz rates. We use 3D-MAP to interrogate neural circuits in 3D and demonstrate simultaneous photostimulation and imaging of dozens of user-selected neurons in the intact mouse brain in vivo with high spatio-temporal resolution. 3D-MAP can be broadly adopted for high-throughput all-optical interrogation of brain circuits owing to its powerful combination of scale, speed, simplicity, and cost.
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spelling doaj.art-2b97d649d2754656b95ef0ad9eca366f2022-12-22T04:32:46ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.73266Three-dimensional multi-site random access photostimulation (3D-MAP)Yi Xue0https://orcid.org/0000-0003-2622-083XLaura Waller1https://orcid.org/0000-0003-1243-2356Hillel Adesnik2https://orcid.org/0000-0002-3796-8643Nicolas Pégard3https://orcid.org/0000-0003-2868-7118Department of Electrical Engineering & Computer Sciences, University of California, Berkeley, Berkeley, United StatesDepartment of Electrical Engineering & Computer Sciences, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular & Cell Biology, University of California, Berkeley, Berkeley, United States; Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United StatesDepartment of Applied Physical Sciences, University of North Carolina at Chapel Hill, Chapel Hill, United States; Department of Biomedical Engineering, University of North Carolina at Chapel Hill, Chapel Hill, United States; UNC Neuroscience Center, University of North Carolina at Chapel Hill, Chapel Hill, United StatesOptical control of neural ensemble activity is crucial for understanding brain function and disease, yet no technology can achieve optogenetic control of very large numbers of neurons at an extremely fast rate over a large volume. State-of-the-art multiphoton holographic optogenetics requires high-power illumination that only addresses relatively small populations of neurons in parallel. Conversely, one-photon holographic techniques can stimulate more neurons with two to three orders lower power, but with limited resolution or addressable volume. Perhaps most problematically, two-photon holographic optogenetic systems are extremely expensive and sophisticated which has precluded their broader adoption in the neuroscience community. To address this technical gap, we introduce a new one-photon light sculpting technique, three-dimensional multi-site random access photostimulation (3D-MAP), that overcomes these limitations by modulating light dynamically, both in the spatial and in the angular domain at multi-kHz rates. We use 3D-MAP to interrogate neural circuits in 3D and demonstrate simultaneous photostimulation and imaging of dozens of user-selected neurons in the intact mouse brain in vivo with high spatio-temporal resolution. 3D-MAP can be broadly adopted for high-throughput all-optical interrogation of brain circuits owing to its powerful combination of scale, speed, simplicity, and cost.https://elifesciences.org/articles/73266light fieldoptogeneticscalcium imagingoptical microscopyneural circuitvisual cortex
spellingShingle Yi Xue
Laura Waller
Hillel Adesnik
Nicolas Pégard
Three-dimensional multi-site random access photostimulation (3D-MAP)
eLife
light field
optogenetics
calcium imaging
optical microscopy
neural circuit
visual cortex
title Three-dimensional multi-site random access photostimulation (3D-MAP)
title_full Three-dimensional multi-site random access photostimulation (3D-MAP)
title_fullStr Three-dimensional multi-site random access photostimulation (3D-MAP)
title_full_unstemmed Three-dimensional multi-site random access photostimulation (3D-MAP)
title_short Three-dimensional multi-site random access photostimulation (3D-MAP)
title_sort three dimensional multi site random access photostimulation 3d map
topic light field
optogenetics
calcium imaging
optical microscopy
neural circuit
visual cortex
url https://elifesciences.org/articles/73266
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AT laurawaller threedimensionalmultisiterandomaccessphotostimulation3dmap
AT hilleladesnik threedimensionalmultisiterandomaccessphotostimulation3dmap
AT nicolaspegard threedimensionalmultisiterandomaccessphotostimulation3dmap