Resting state functional connectivity in the human spinal cord

Barry, Robert; Smith, Seth A.; Dula, Adrienne N.; Gore, John C.

doi:10.7554/elife.02812

Cited by 105 publications

(203 citation statements)

References 57 publications

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“…Spinal gray matter horns are highly functionally connected at rest, to a much greater degree than has been previously recognized. Strong dorsal horn-to-horn connectivity was found in our study in anesthetized monkeys as well as in the two very recent studies in awake humans using different analytic methods (6,7). However, the specific horn-to-horn functional connectivity patterns within and across segments varied from the current study.…”

Section: Discussion Widespread Fmri Responses To Noxious Stimuli Withsupporting

confidence: 47%

“…The current study extends these ideas from the brain to the spinal cord. Our findings indicate that baseline functional connectivity is a common organizational feature within the central nervous system (6,7,30). Spinal gray matter horns are highly functionally connected at rest, to a much greater degree than has been previously recognized.…”

Section: Discussion Widespread Fmri Responses To Noxious Stimuli Withsupporting

confidence: 46%

“…More importantly, alterations of rsFC networks in various disease conditions have altered our view about the functional significance of spontaneous baseline neural activity (3). Two very recent reports of success in detecting intrinsic functional circuits in human spines using resting-state fMRI once more suggest that rsFC is a fundamental, common feature of the entire nervous system (6,7).…”

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confidence: 99%

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Injury alters intrinsic functional connectivity within the primate spinal cord

Chen

Mishra²,

Yang³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Recent demonstrations of correlated low-frequency MRI signal variations between subregions of the spinal cord at rest in humans, similar to those found in the brain, suggest that such resting-state functional connectivity constitutes a common feature of the intrinsic organization of the entire central nervous system. We report our detection of functional connectivity within the spinal cords of anesthetized squirrel monkeys at rest and show that the strength of connectivity within these networks is altered by the effects of injuries. By quantifying the low-frequency MRI signal correlations between different horns within spinal cord gray matter, we found distinct functional connectivity relationships between the different sensory and motor horns, a pattern that was similar to activation patterns evoked by nociceptive heat or tactile stimulation of digits. All horns within a single spinal segment were functionally connected, with the strongest connectivity occurring between ipsilateral dorsal and ventral horns. Each horn was strongly connected to the same horn on neighboring segments, but this connectivity reduced drastically along the spinal cord. Unilateral injury to the spinal cord significantly weakened the strength of the intrasegment horn-to-horn connectivity only on the injury side and in slices below the lesion. These findings suggest resting-state functional connectivity may be a useful biomarker of functional integrity in injured and recovering spinal cords.hand | spinal cord injury | resting state fMRI | monkey | cervical spinal cord R esting-state functional connectivity (rsFC) has been widely used to identify and characterize neural circuits in the brain (1-3), and its presentation at various spatial scales and its changes with specific physiological conditions confirm its fundamental role in maintaining normal brain function (4, 5). More importantly, alterations of rsFC networks in various disease conditions have altered our view about the functional significance of spontaneous baseline neural activity (3). Two very recent reports of success in detecting intrinsic functional circuits in human spines using resting-state fMRI once more suggest that rsFC is a fundamental, common feature of the entire nervous system (6, 7).Despite these exciting findings in human subjects, the functional and behavioral relevance of the intrinsic functional networks within the spine gray matter remains largely obscure, and there have been no previous reports attempting to understand their significance. One way to address this question is to manipulate the network and then examine how the network reacts to the manipulation. This type of approach is impossible to execute in humans but can be performed in nonhuman primates in a very well-controlled manner. Thus, this study aimed to better understand the functional and behavioral relevance of newly identified rsFC in the spinal cord by first determining whether similar intrinsic rsFC networks can be detected in the spinal cords of anesthetized monkeys. We also sought to determ...

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Section: Discussion Widespread Fmri Responses To Noxious Stimuli Withsupporting

confidence: 47%

Section: Discussion Widespread Fmri Responses To Noxious Stimuli Withsupporting

confidence: 46%

mentioning

confidence: 99%

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Injury alters intrinsic functional connectivity within the primate spinal cord

Chen

Mishra²,

Yang³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…This finding is interesting with regard to a seed-based resting-state study that observed stronger connectivity between ventral horns than dorsal horns (28) and two previous task-based spinal fMRI studies that showed a strong bilateral activation during motor tasks (43), but a clearly lateralized activation during painful sensory stimulation (37). Although such correspondence between task-related and resting-state spinal fMRI signals might be incidental, there is also evidence for a close correspondence of task-related and resting-state networks in the brain (10).…”

Section: Discussionmentioning

confidence: 81%

Intrinsically organized resting state networks in the human spinal cord

Kong

Eippert

Beckmann

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

144

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Spontaneous fluctuations in functional magnetic resonance imaging (fMRI) signals of the brain have repeatedly been observed when no task or external stimulation is present. These fluctuations likely reflect baseline neuronal activity of the brain and correspond to functionally relevant resting-state networks (RSN). It is not known however, whether intrinsically organized and spatially circumscribed RSNs also exist in the spinal cord, the brain's principal sensorimotor interface with the body. Here, we use recent advances in spinal fMRI methodology and independent component analysis to answer this question in healthy human volunteers. We identified spatially distinct RSNs in the human spinal cord that were clearly separated into dorsal and ventral components, mirroring the functional neuroanatomy of the spinal cord and likely reflecting sensory and motor processing. Interestingly, dorsal (sensory) RSNs were separated into right and left components, presumably related to ongoing hemibody processing of somatosensory information, whereas ventral (motor) RSNs were bilateral, possibly related to commissural interneuronal networks involved in central pattern generation. Importantly, all of these RSNs showed a restricted spatial extent along the spinal cord and likely conform to the spinal cord's functionally relevant segmental organization. Although the spatial and temporal properties of the dorsal and ventral RSNs were found to be significantly different, these networks showed significant interactions with each other at the segmental level. Together, our data demonstrate that intrinsically highly organized resting-state fluctuations exist in the human spinal cord and are thus a hallmark of the entire central nervous system. fMRI | spinal cord | resting state | connectivity | networks F unctional magnetic resonance imaging (fMRI) has been used to study the functional connectivity of the human brain, with spontaneous fluctuations in the resting-state fMRI signal (1-3) attracting much attention in the past few years (for review, see refs. 4-6). Brain regions showing temporally coherent spontaneous fluctuations constitute several anatomically consistent "resting state networks" (RSNs), such as visual, auditory, sensorymotor, executive control, and default mode networks (7-11). Consequently, analyses of RSNs are rapidly emerging as a powerful tool for in vivo mapping of neural circuitry in the human brain and one such approach for exploring RSNs is independent component analysis (ICA) (12)(13)(14). ICA decomposes the data into spatially independent and temporally coherent source signals/ components. The advantage of ICA over more traditional seedbased approaches (15) is that it is a model-free, data-driven multiple-regression approach, i.e., within the ICA framework we can account for multiple underlying signal contributions (artifactual or neuronal in origin) simultaneously and thereby disentangle these different contributions to the measured observations (16). To date, ICA has been used not only to characterize brain con...

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“…Performing it before temporal filtering is acceptable, but performing it after temporal filtering will lead to reintroduction of noise into the timeseries and inflated correlations; if it is necessary for nuisance regression to be performed after temporal filtering, then one should apply the same filter to the nuisance regressors themselves. It is reassuring to see that previous spinal cord resting-state studies did not fall prey to this mistake when using nuisance regression (Barry et al, 2016(Barry et al, , 2014Kong et al, 2014). Second, the use of low-pass or bandpass filtering is questionable, as several recent brain imaging studies have shown that frequencies above the common cut-off of 0.1Hz do contain meaningful signal (e.g.…”

Section: Discussionmentioning

confidence: 99%

Denoising spinal cord fMRI data: Approaches to acquisition and analysis

et al. 2017

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General rightsThis document is made available in accordance with publisher policies. Please cite only the published version using the reference above. AbstractFunctional magnetic resonance imaging (fMRI) of the human spinal cord is a difficult endeavour due to the cord's small cross-sectional diameter, signal drop-out as well as image distortion due to magnetic field inhomogeneity, and the confounding influence of physiological noise from cardiac and respiratory sources. Nevertheless, there is great interest in spinal fMRI due to the spinal cord's role as the principal sensorimotor interface between the brain and the body and its involvement in a variety of sensory and motor pathologies. In this review, we give an overview of the various methods that have been used to address the technical challenges in spinal fMRI, with a focus on reducing the impact of physiological noise. We start out by describing acquisition methods that have been tailored to the special needs of spinal cord fMRI and aim to increase the signal-to-noise ratio and reduce distortion in obtained images. Following this, we concentrate on image processing and analysis approaches that address the detrimental effects of noise. While these include variations of standard pre-processing methods such as motion correction and spatial filtering, the main focus lies on denoising techniques that can be applied to taskbased as well as resting-state data sets. We review both model-based approaches that rely on externally acquired respiratory and cardiac signals as well as data-driven approaches that estimate and correct for noise using the data themselves. We conclude with an outlook on techniques that have been successfully applied for noise reduction in brain imaging and whose use might be beneficial for fMRI of the human spinal cord.3

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Resting state functional connectivity in the human spinal cord

Cited by 105 publications

References 57 publications

Injury alters intrinsic functional connectivity within the primate spinal cord

Injury alters intrinsic functional connectivity within the primate spinal cord

Intrinsically organized resting state networks in the human spinal cord

Denoising spinal cord fMRI data: Approaches to acquisition and analysis

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