An orderly sequence of autonomic and neural events at transient arousal changes
Resting-state functional magnetic resonance imaging (rsfMRI) allows the study of functional brain connectivity based on spatially structured variations in neuronal activity. Proper evaluation of connectivity requires removal of non-neural contributions to the fMRI signal, in particular hemodynamic c...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-12-01
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| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922008412 |
| _version_ | 1811294383747629056 |
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| author | Yameng Gu Feng Han Lucas E. Sainburg Margeaux M. Schade Orfeu M. Buxton Jeff H. Duyn Xiao Liu |
| author_facet | Yameng Gu Feng Han Lucas E. Sainburg Margeaux M. Schade Orfeu M. Buxton Jeff H. Duyn Xiao Liu |
| author_sort | Yameng Gu |
| collection | DOAJ |
| description | Resting-state functional magnetic resonance imaging (rsfMRI) allows the study of functional brain connectivity based on spatially structured variations in neuronal activity. Proper evaluation of connectivity requires removal of non-neural contributions to the fMRI signal, in particular hemodynamic changes associated with autonomic variability. Regression analysis based on autonomic indicator signals has been used for this purpose, but may be inadequate if neuronal and autonomic activities covary. To investigate this potential co-variation, we performed rsfMRI experiments while concurrently acquiring electroencephalography (EEG) and autonomic indicator signals, including heart rate, respiratory depth, and peripheral vascular tone. We identified a recurrent and systematic spatiotemporal pattern of fMRI (named as fMRI cascade), which features brief signal reductions in salience and default-mode networks and the thalamus, followed by a biphasic global change with a sensory-motor dominance. This fMRI cascade, which was mostly observed during eyes-closed condition, was accompanied by large EEG and autonomic changes indicative of arousal modulations. Importantly, the removal of the fMRI cascade dynamics from rsfMRI diminished its correlations with various signals. These results suggest that the rsfMRI correlations with various physiological and neural signals are not independent but arise, at least partly, from the fMRI cascades and associated neural and physiological changes at arousal modulations. |
| first_indexed | 2024-04-13T05:16:45Z |
| format | Article |
| id | doaj.art-8bd1c05fbb3043cfb60f56a4143af87b |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-04-13T05:16:45Z |
| publishDate | 2022-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-8bd1c05fbb3043cfb60f56a4143af87b2022-12-22T03:00:52ZengElsevierNeuroImage1095-95722022-12-01264119720An orderly sequence of autonomic and neural events at transient arousal changesYameng Gu0Feng Han1Lucas E. Sainburg2Margeaux M. Schade3Orfeu M. Buxton4Jeff H. Duyn5Xiao Liu6Department of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802, USADepartment of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802, USADepartment of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802, USADepartment of Biobehavioral Health, The Pennsylvania State University, University Park, PA 16802, USADepartment of Biobehavioral Health, The Pennsylvania State University, University Park, PA 16802, USAAdvanced MRI Section, Laboratory of Functional and Molecular Imaging, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USADepartment of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802, USA; Institute for Computational and Data Sciences, The Pennsylvania State University, University Park, PA 16802, USA; Corresponding author at: 431 Chemical and Biomedical Engineering Building, The Pennsylvania State University, University Park, PA 16802-4400, USA.Resting-state functional magnetic resonance imaging (rsfMRI) allows the study of functional brain connectivity based on spatially structured variations in neuronal activity. Proper evaluation of connectivity requires removal of non-neural contributions to the fMRI signal, in particular hemodynamic changes associated with autonomic variability. Regression analysis based on autonomic indicator signals has been used for this purpose, but may be inadequate if neuronal and autonomic activities covary. To investigate this potential co-variation, we performed rsfMRI experiments while concurrently acquiring electroencephalography (EEG) and autonomic indicator signals, including heart rate, respiratory depth, and peripheral vascular tone. We identified a recurrent and systematic spatiotemporal pattern of fMRI (named as fMRI cascade), which features brief signal reductions in salience and default-mode networks and the thalamus, followed by a biphasic global change with a sensory-motor dominance. This fMRI cascade, which was mostly observed during eyes-closed condition, was accompanied by large EEG and autonomic changes indicative of arousal modulations. Importantly, the removal of the fMRI cascade dynamics from rsfMRI diminished its correlations with various signals. These results suggest that the rsfMRI correlations with various physiological and neural signals are not independent but arise, at least partly, from the fMRI cascades and associated neural and physiological changes at arousal modulations.http://www.sciencedirect.com/science/article/pii/S1053811922008412Arousal modulationsAutonomic activityMultimodal neuroimagingResting-state fMRI |
| spellingShingle | Yameng Gu Feng Han Lucas E. Sainburg Margeaux M. Schade Orfeu M. Buxton Jeff H. Duyn Xiao Liu An orderly sequence of autonomic and neural events at transient arousal changes NeuroImage Arousal modulations Autonomic activity Multimodal neuroimaging Resting-state fMRI |
| title | An orderly sequence of autonomic and neural events at transient arousal changes |
| title_full | An orderly sequence of autonomic and neural events at transient arousal changes |
| title_fullStr | An orderly sequence of autonomic and neural events at transient arousal changes |
| title_full_unstemmed | An orderly sequence of autonomic and neural events at transient arousal changes |
| title_short | An orderly sequence of autonomic and neural events at transient arousal changes |
| title_sort | orderly sequence of autonomic and neural events at transient arousal changes |
| topic | Arousal modulations Autonomic activity Multimodal neuroimaging Resting-state fMRI |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922008412 |
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