Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice

Brain function originates from hierarchical spatial-temporal neural dynamics distributed across cortical and subcortical networks. However, techniques available to assess large-scale brain network activity with single-neuron resolution in behaving animals remain limited. Here, we present Mesotrode t...

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Main Authors: Dongsheng Xiao, Yuhao Yan, Timothy H Murphy
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/87691
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author Dongsheng Xiao
Yuhao Yan
Timothy H Murphy
author_facet Dongsheng Xiao
Yuhao Yan
Timothy H Murphy
author_sort Dongsheng Xiao
collection DOAJ
description Brain function originates from hierarchical spatial-temporal neural dynamics distributed across cortical and subcortical networks. However, techniques available to assess large-scale brain network activity with single-neuron resolution in behaving animals remain limited. Here, we present Mesotrode that integrates chronic wide-field mesoscale cortical imaging and compact multi-site cortical/subcortical cellular electrophysiology in head-fixed mice that undergo self-initiated running or orofacial movements. Specifically, we harnessed the flexibility of chronic multi-site tetrode recordings to monitor single-neuron activity in multiple subcortical structures while simultaneously imaging the mesoscale activity of the entire dorsal cortex. A mesoscale spike-triggered averaging procedure allowed the identification of cortical activity motifs preferentially associated with single-neuron spiking. Using this approach, we were able to characterize chronic single-neuron-related functional connectivity maps for up to 60 days post-implantation. Neurons recorded from distinct subcortical structures display diverse but segregated cortical maps, suggesting that neurons of different origins participate in distinct cortico-subcortical pathways. We extended the capability of Mesotrode by implanting the micro-electrode at the facial motor nerve and found that facial nerve spiking is functionally associated with the PTA, RSP, and M2 network, and optogenetic inhibition of the PTA area significantly reduced the facial movement of the mice. These findings demonstrate that Mesotrode can be used to sample different combinations of cortico-subcortical networks over prolonged periods, generating multimodal and multi-scale network activity from a single implant, offering new insights into the neural mechanisms underlying specific behaviors.
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spelling doaj.art-c80f609f92fa4006a5adfbb137410cb62023-11-15T15:46:34ZengeLife Sciences Publications LtdeLife2050-084X2023-11-011210.7554/eLife.87691Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in miceDongsheng Xiao0https://orcid.org/0000-0002-1669-0021Yuhao Yan1Timothy H Murphy2https://orcid.org/0000-0002-0093-4490University of British Columbia, Department of Psychiatry, Kinsmen Laboratory of Neurological Research, Vancouver, Canada; Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, CanadaUniversity of British Columbia, Department of Psychiatry, Kinsmen Laboratory of Neurological Research, Vancouver, Canada; Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, CanadaUniversity of British Columbia, Department of Psychiatry, Kinsmen Laboratory of Neurological Research, Vancouver, Canada; Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, CanadaBrain function originates from hierarchical spatial-temporal neural dynamics distributed across cortical and subcortical networks. However, techniques available to assess large-scale brain network activity with single-neuron resolution in behaving animals remain limited. Here, we present Mesotrode that integrates chronic wide-field mesoscale cortical imaging and compact multi-site cortical/subcortical cellular electrophysiology in head-fixed mice that undergo self-initiated running or orofacial movements. Specifically, we harnessed the flexibility of chronic multi-site tetrode recordings to monitor single-neuron activity in multiple subcortical structures while simultaneously imaging the mesoscale activity of the entire dorsal cortex. A mesoscale spike-triggered averaging procedure allowed the identification of cortical activity motifs preferentially associated with single-neuron spiking. Using this approach, we were able to characterize chronic single-neuron-related functional connectivity maps for up to 60 days post-implantation. Neurons recorded from distinct subcortical structures display diverse but segregated cortical maps, suggesting that neurons of different origins participate in distinct cortico-subcortical pathways. We extended the capability of Mesotrode by implanting the micro-electrode at the facial motor nerve and found that facial nerve spiking is functionally associated with the PTA, RSP, and M2 network, and optogenetic inhibition of the PTA area significantly reduced the facial movement of the mice. These findings demonstrate that Mesotrode can be used to sample different combinations of cortico-subcortical networks over prolonged periods, generating multimodal and multi-scale network activity from a single implant, offering new insights into the neural mechanisms underlying specific behaviors.https://elifesciences.org/articles/87691mesoscale cortical imagingsubcorticalcircuitperipheral nerveoptogeneticssystems modeling
spellingShingle Dongsheng Xiao
Yuhao Yan
Timothy H Murphy
Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice
eLife
mesoscale cortical imaging
subcortical
circuit
peripheral nerve
optogenetics
systems modeling
title Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice
title_full Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice
title_fullStr Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice
title_full_unstemmed Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice
title_short Mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice
title_sort mesotrode allows chronic simultaneous mesoscale cortical imaging and subcortical or peripheral nerve spiking activity recording in mice
topic mesoscale cortical imaging
subcortical
circuit
peripheral nerve
optogenetics
systems modeling
url https://elifesciences.org/articles/87691
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AT yuhaoyan mesotrodeallowschronicsimultaneousmesoscalecorticalimagingandsubcorticalorperipheralnervespikingactivityrecordinginmice
AT timothyhmurphy mesotrodeallowschronicsimultaneousmesoscalecorticalimagingandsubcorticalorperipheralnervespikingactivityrecordinginmice