A Functional Magnetic Resonance Imaging Study of Head Movements in Cervical Dystonia

Prudente, Cecília N.; Stilla, Randall; Singh, Shivangi; Buetefisch, Cathrin M.; Evatt, Marian L.; Factor, Stewart A.; Freeman, Alan; Hu, Xiaoping; Hess, Ellen J.; Sathian, K.; Jinnah, Hyder A.

doi:10.3389/fneur.2016.00201

Cited by 31 publications

(39 citation statements)

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“…Supporting the notion that CD is a network disorder [Battistella et al, 2017;Lehericy et al, 2013;Neychev et al, 2011;Prudente et al, 2014], the observed functional alterations of intra-and inter-regional measurements are consistent with previous studies reporting a wide distribution of structural [Prell et al, 2013;Ramdhani et al, 2014] and functional [de Vries et al, 2008;Prudente et al, 2016] alterations in the basal ganglia, thalamus, cerebellum, sensorimotor cortex, and other cortical regions. Particularly, a previous review [Neychev et al, 2011] has pointed out that dystonia may result from combined dysfunction of multiple nodes or from aberrant communications among them; but which of these possibilities best applies to dystonia remains unclear.…”

Section: Discussionsupporting

confidence: 90%

Alterations of resting‐state fMRI measurements in individuals with cervical dystonia

Prudente

Stilla

et al. 2017

Human Brain Mapping

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Cervical dystonia (CD) is a neurological disorder with typical symptoms of involuntary and abnormal movements and postures of the head. CD-associated alterations of functional brain networks have not been well characterized. Previous studies of CD using resting-state functional MRI (rfMRI) are limited in 2 aspects: (i) the analyses were not directly focused on the functional brain network related to head movement and (ii) rfMRI measurements other than functional connectivity (FC) were not investigated. The present study examined alterations of FC in CD by capitalizing on newly identified brain regions supporting isometric head rotation (Prudente et al., 2015). In addition to FC, which only reflects inter-regional signal synchronization, local or intra-regional alterations were also examined using rfMRI measurements of the fractional amplitude of low frequency fluctuations (fALFF) and regional homogeneity (ReHo). Finally, with alterations of different rfMRI measures identified, a support vector machine (SVM) learning algorithm was implemented for group classification. The results revealed both inter-(FC) and intra-regional (ReHo) alterations extensively distributed in both cortical and subcortical structures; and common alterations of these measures were identified bilaterally in the postcentral gyrus as well as in the basal ganglia and thalamus. Of the rfMRI features examined, 7 of them (4 FC and 3 ReHo measures) survived the SVM procedure of recursive feature elimination and together provided the highest group classification accuracy of 90.6%. The present findings extend previous studies of rfMRI in CD and offer insight into the underlying pathophysiology of the disorder in relation to network dysfunction and somatosensory disturbances.

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Section: Discussionsupporting

confidence: 90%

Alterations of resting‐state fMRI measurements in individuals with cervical dystonia

Prudente

Stilla

et al. 2017

Human Brain Mapping

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“…3A). Medial and lateral clusters were found within the somatosensory cortex, consistent with previous reports of both a medial and lateral representation for the neck within the homunculus (Prudente et al, 2015(Prudente et al, , 2016. Some smaller clusters of (positive and negative) functionally connected voxels were also present ( Supplementary Fig.…”

Section: Lesion Network Mappingsupporting

confidence: 90%

“…Our cerebellar and somatosensory regions of interest were used as seed regions to compare functional connectivity patterns between 39 idiopathic cervical dystonia patients and 37 control subjects, in a dataset collated from two previously published rs-fcMRI studies of idiopathic cervical dystonia (Delnooz et al, 2013;Prudente et al, 2016). The preprocessing of the rs-fcMRI data followed conventional methods and guidelines, including global signal regression (Fox et al, 2010;Murphy et al, 2016), but added an extra artefact-reduction step modified from prior principal component analysis-based approaches (Behzadi et al, 2007)…”

Section: Relevance To Idiopathic Cervical Dystoniamentioning

confidence: 99%

“…Cervical dystonia is a chronic neurological disorder characterized by sustained and involuntary contractions of the neck muscles, and is the most common form of focal dystonia (Xiao et al, 2012). Cervical dystonia has traditionally been ascribed to dysfunction of the basal ganglia (Galardi et al, 1996;Naumann et al, 1998), but abnormalities have been observed in many other brain regions including the cerebellum (Batla et al, 2015), prefrontal cortex , midbrain (Holmes et al, 2012), motor cortex (Richardson, 2015), and somatosensory cortex (Prudente et al, 2016). This has led to the suggestion that cervical dystonia is a 'network disorder' resulting from dysfunction in multiple different brain regions (Jinnah et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Network localization of cervical dystonia based on causal brain lesions

Corp

Joutsa

Darby

et al. 2019

Brain

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These authors contributed equally to this work.Cervical dystonia is a neurological disorder characterized by sustained, involuntary movements of the head and neck. Most cases of cervical dystonia are idiopathic, with no obvious cause, yet some cases are acquired, secondary to focal brain lesions. These latter cases are valuable as they establish a causal link between neuroanatomy and resultant symptoms, lending insight into the brain regions causing cervical dystonia and possible treatment targets. However, lesions causing cervical dystonia can occur in multiple different brain locations, leaving localization unclear. Here, we use a technique termed 'lesion network mapping', which uses connectome data from a large cohort of healthy subjects (resting state functional MRI, n = 1000) to test whether lesion locations causing cervical dystonia map to a common brain network. We then test whether this network, derived from brain lesions, is abnormal in patients with idiopathic cervical dystonia (n = 39) versus matched controls (n = 37). A systematic literature search identified 25 cases of lesion-induced cervical dystonia. Lesion locations were heterogeneous, with lesions scattered throughout the cerebellum, brainstem, and basal ganglia. However, these heterogeneous lesion locations were all part of a single functionally connected brain network. Positive connectivity to the cerebellum and negative connectivity to the somatosensory cortex were specific markers for cervical dystonia compared to lesions causing other neurological symptoms. Connectivity with these two regions defined a single brain network that encompassed the heterogeneous lesion locations causing cervical dystonia. These cerebellar and somatosensory regions also showed abnormal connectivity in patients with idiopathic cervical dystonia. Finally, the most effective deep brain stimulation sites for treating dystonia were connected to these same cerebellar and somatosensory regions identified using lesion network mapping. These results lend insight into the causal neuroanatomical substrate of cervical dystonia, demonstrate convergence across idiopathic and acquired dystonia, and identify a network target for dystonia treatment. Abbreviations: DBS = deep brain stimulation; rs-fcMRI = resting state functional connectivity MRI Brain network of cervical dystonia

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“…Specifically, the increased severity of dystonic symptoms was associated with reduced functional activity in S1 and increased functional activity in the anterior portion of the cerebellum. A recent fMRI study in CD revealed that head rotation in the direction of dystonic head rotation is related to hyperactivity in the anterior cerebellum and that head rotation in the opposite direction is associated with increased activity in the sensorimotor cortex [Prudente et al, 2016]. Together, these findings reinforce the view that both cortical and subcortical sensorimotor abnormalities are likely to contribute to dystonic symptoms in this patient population [Løkkegaard et al, 2016;Prudente et al, 2014], and both S1 and cerebellum could be targets for intervention in studies looking for ways to reduce symptoms in CD.…”

Section: Discussionmentioning

confidence: 99%

Functional activity of the sensorimotor cortex and cerebellum relates to cervical dystonia symptoms

et al. 2017

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Cervical dystonia (CD) is the most common type of focal dystonia, causing abnormal movements of the neck and head. In this study we used noninvasive imaging to investigate the motor system of patients with CD and uncover the neural correlates of dystonic symptoms. Furthermore, we examined whether a commonly prescribed anticholinergic medication in CD has an effect on the dystonia-related brain abnormalities. Participants included 16 patients with CD and 16 healthy age-matched controls. We collected functional MRI scans during a force task previously shown to extensively engage the motor system, and diffusion and T1-weighted MRI scans from which we calculated free-water and brain tissue densities. The dystonia group was also scanned ca. 2 hours after a 2-mg dose of trihexyphenidyl. Severity of dystonia was assessed pre- and post-drug using the Burke-Fahn-Marsden Dystonia Rating Scale. Motor-related activity in CD was altered relative to controls in the primary somatosensory cortex, cerebellum, dorsal premotor and posterior parietal cortices, and occipital cortex. Most importantly, a regression model showed that increased severity of symptoms was associated with decreased functional activity of the somatosensory cortex and increased activity of the cerebellum. Structural imaging measures did not differ between CD and controls. The single dose of trihexyphenidyl altered the fMRI signal in the somatosensory cortex but not in the cerebellum. Symptom severity was not significantly reduced post-treatment. Findings show widespread changes in functional brain activity in CD and most importantly that dystonic symptoms relate to disrupted activity in the somatosensory cortex and cerebellum.

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A Functional Magnetic Resonance Imaging Study of Head Movements in Cervical Dystonia

Cited by 31 publications

References 58 publications

Alterations of resting‐state fMRI measurements in individuals with cervical dystonia

Alterations of resting‐state fMRI measurements in individuals with cervical dystonia

Network localization of cervical dystonia based on causal brain lesions

Functional activity of the sensorimotor cortex and cerebellum relates to cervical dystonia symptoms

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