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      Intrinsic functional architecture of the non-human primate spinal cord derived from fMRI and electrophysiology

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          Abstract

          Resting-state functional MRI (rsfMRI) has recently revealed correlated signals in the spinal cord horns of monkeys and humans. However, the interpretation of these rsfMRI correlations as indicators of functional connectivity in the spinal cord remains unclear. Here, we recorded stimulus-evoked and spontaneous spiking activity and local field potentials (LFPs) from monkey spinal cord in order to validate fMRI measures. We found that both BOLD and electrophysiological signals elicited by tactile stimulation co-localized to the ipsilateral dorsal horn. Temporal profiles of stimulus-evoked BOLD signals covaried with LFP and multiunit spiking in a similar way to those observed in the brain. Functional connectivity of dorsal horns exhibited a U-shaped profile along the dorsal-intermediate-ventral axis. Overall, these results suggest that there is an intrinsic functional architecture within the gray matter of a single spinal segment, and that rsfMRI signals at high field directly reflect this underlying spontaneous neuronal activity.

          Abstract

          Resting-state fMRI shows networks of correlated activity in the spinal cord, similar to those in the brain, but whether fMRI is a valid measure of functional connectivity in spinal cord is unclear. Here, the authors show that fMRI corresponds well to electrophysiological measures of spinal cord activity.

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          Most cited references29

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          Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex.

          Functional magnetic resonance imaging (fMRI) is an important tool for investigating human brain function, but the relationship between the hemodynamically based fMRI signals in the human brain and the underlying neuronal activity is unclear. We recorded single unit activity and local field potentials in auditory cortex of two neurosurgical patients and compared them with the fMRI signals of 11 healthy subjects during presentation of an identical movie segment. The predicted fMRI signals derived from single units and the measured fMRI signals from auditory cortex showed a highly significant correlation (r = 0.75, P < 10(-47)). Thus, fMRI signals can provide a reliable measure of the firing rate of human cortical neurons.
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            Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1.

            Most functional brain imaging studies use task-induced hemodynamic responses to infer underlying changes in neuronal activity. In addition to increases in cerebral blood flow and blood oxygenation level-dependent (BOLD) signals, sustained negative responses are pervasive in functional imaging. The origin of negative responses and their relationship to neural activity remain poorly understood. Through simultaneous functional magnetic resonance imaging and electrophysiological recording, we demonstrate a negative BOLD response (NBR) beyond the stimulated regions of visual cortex, associated with local decreases in neuronal activity below spontaneous activity, detected 7.15 +/- 3.14 mm away from the closest positively responding region in V1. Trial-by-trial amplitude fluctuations revealed tight coupling between the NBR and neuronal activity decreases. The NBR was associated with comparable decreases in local field potentials and multiunit activity. Our findings indicate that a significant component of the NBR originates in neuronal activity decreases.
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              Three-Dimensional Reconstruction and Segmentation of Intact Drosophila by Ultramicroscopy

              Genetic mutants are invaluable for understanding the development, physiology and behaviour of Drosophila. Modern molecular genetic techniques enable the rapid generation of large numbers of different mutants. To phenotype these mutants sophisticated microscopy techniques are required, ideally allowing the 3D-reconstruction of the anatomy of an adult fly from a single scan. Ultramicroscopy enables up to cm fields of view, whilst providing micron resolution. In this paper, we present ultramicroscopy reconstructions of the flight musculature, the nervous system, and the digestive tract of entire, chemically cleared, drosophila in autofluorescent light. The 3D-reconstructions thus obtained verify that the anatomy of a whole fly, including the filigree spatial organization of the direct flight muscles, can be analysed from a single ultramicroscopy reconstruction. The recording procedure, including 3D-reconstruction using standard software, takes no longer than 30 min. Additionally, image segmentation, which would allow for further quantitative analysis, was performed.
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                Author and article information

                Contributors
                tung-lin.wu@vanderbilt.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                29 March 2019
                29 March 2019
                2019
                : 10
                : 1416
                Affiliations
                [1 ]ISNI 0000 0001 2264 7217, GRID grid.152326.1, Vanderbilt University Institute of Imaging Science, ; Nashville, TN 37232 USA
                [2 ]ISNI 0000 0001 2264 7217, GRID grid.152326.1, Biomedical Engineering, Vanderbilt University, ; Nashville, TN 37232 USA
                [3 ]ISNI 0000 0004 1936 9916, GRID grid.412807.8, Radiology and Radiological Sciences, Vanderbilt University Medical Center, ; Nashville, TN 37232 USA
                [4 ]ISNI 0000 0001 2264 7217, GRID grid.152326.1, Department of Physics and Astronomy, , Vanderbilt University, ; Nashville, TN 37232 USA
                Author information
                http://orcid.org/0000-0002-8965-7708
                http://orcid.org/0000-0001-9662-1925
                Article
                9485
                10.1038/s41467-019-09485-3
                6440970
                30926817
                b11ff737-f030-4f8b-ae66-a9f64c6a8776
                © This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2019 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 7 October 2018
                : 5 March 2019
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