Adaptation of feedforward movement control is abnormal in patients with cervical dystonia and tremor

Avanzino, Laura; Ravaschio, Andrea; Lagravinese, Giovanna; Bonassi, Gaia; Abbruzzese, Giovanni; Pelosin, Elisa

doi:10.1016/j.clinph.2017.08.020

Cited by 27 publications

(15 citation statements)

References 43 publications

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“…Several studies have found normal cerebellar function or connectivity in idiopathic cervical dystonia patients, or abnormal cerebellar function only in cervical dystonia patients with tremor (Delnooz et al, 2013;Sadnicka et al, 2014;Antelmi et al, 2016;Bologna et al, 2016;Avanzino et al, 2018). Here, we found that all lesions causing cervical dystonia were connected to the cerebellum, including cases with no head tremor ( Supplementary Fig.…”

Section: The Cerebellum In Cervical Dystoniasupporting

confidence: 59%

Network localization of cervical dystonia based on causal brain lesions

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Joutsa

Darby

et al. 2019

Brain

180

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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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Section: The Cerebellum In Cervical Dystoniasupporting

confidence: 59%

Network localization of cervical dystonia based on causal brain lesions

Corp

Joutsa

Darby

et al. 2019

Brain

180

177

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“…It is therefore possible that proprioceptive afferent information flowing from the cerebellum in CD and FHD competes, once it reaches the thalamus, with tactile information during index finger movements, thereby altering the timing of tactile sensory processing gating. Concordantly recent evidence suggests a role of the cerebellum in the pathophysiological mechanisms of dystonia . The observation that movement velocity in patients with CD and FHD did not vary during the sensorimotor integration task suggests that there might be an unbalanced interplay in these patients between motor and sensory information in favor of motor output, with an excessive degree of gating on tactile information.…”

Section: Discussionmentioning

confidence: 62%

“…Concordantly recent evidence suggests a role of the cerebellum in the pathophysiological mechanisms of dystonia. [42][43][44][45] The observation that movement velocity in patients with CD and FHD did not vary during the sensorimotor integration task suggests that there might be an unbalanced interplay in these patients between motor and sensory information in favor of motor output, with an excessive degree of gating on tactile information. As tactile information gating may promote movement arrest, excessive tactile gating may reduce the likelihood of the movement ceasing.…”

Section: Discussionmentioning

confidence: 97%

Abnormal sensory gating in patients with different types of focal dystonias

et al. 2018

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Background Movement execution in healthy individuals increases the somatosensory temporal discrimination threshold. These changes are a result of mechanisms of sensory gating at the subcortical level. Although the somatosensory temporal discrimination threshold is abnormally increased in patients with focal dystonias, the effect of movement execution on somatosensory temporal discrimination in dystonic patients is unknown. Objectives The objective of this study was to determine whether somatosensory temporal discrimination threshold modulation induced by voluntary movement is normal in different forms of focal dystonia. Methods We enrolled 71 dystonic patients (24 with blepharospasm, 31 with cervical dystonia, and 16 with focal hand dystonia) and 39 age‐matched healthy participants. Paired stimuli for the somatosensory temporal discrimination threshold were triggered by movement execution at movement onset and at various time intervals thereafter. We analyzed the kinematic features of the motor task to ascertain whether tactile input induces changes in movement parameters. Results Movement execution led to greater and longer lasting increases in somatosensory temporal discrimination threshold values, both upon movement onset and at various time intervals thereafter, in patients with cervical dystonia and focal hand dystonia than in those with blepharospasm or the healthy participants. Somatosensory temporal discrimination testing did not induce any changes in the mean velocity of index finger movements in either patients or healthy participants. Conclusions Somatosensory temporal discrimination threshold changes induced by movement execution are abnormal in focal dystonias. This abnormality is related to the type of dystonia. Abnormal gating of sensory information is likely involved in movement‐induced triggering or worsening of different forms focal dystonia. © 2018 International Parkinson and Movement Disorder Society

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“…Taken together, such deficits may be linked to an abnormal internal model of motor commands reflecting dysfunction of cerebellar outflow pathways. Consistent with this hypothesis, Avanzino and co-workers have recently demonstrated deficits in anticipatory movement control in patients with cervical dystonia [240]. The term 'anticipatory' indicates the feed-forward portion of a movement that is planned in advance and relies on the internal model of motor act.…”

Section: Dystoniamentioning

confidence: 84%

Consensus paper: Decoding the Contributions of the Cerebellum as a Time Machine. From Neurons to Clinical Applications

et al. 2018

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Time perception is an essential element of conscious and subconscious experience, coordinating our perception and interaction with the surrounding environment. In recent years, major technological advances in the field of neuroscience have helped foster new insights into the processing of temporal information, including extending our knowledge of the role of the cerebellum as one of the key nodes in the brain for this function. This consensus paper provides a state-of-the-art picture from the experts in the field of the cerebellar research on a variety of crucial issues related to temporal processing, drawing on recent anatomical, neurophysiological, behavioral, and clinical research.The cerebellar granular layer appears especially well-suited for timing operations required to confer millisecond precision for cerebellar computations. This may be most evident in the manner the cerebellum controls the duration of the timing of agonist-antagonist EMG bursts associated with fast goal-directed voluntary movements. In concert with adaptive processes, interactions within the cerebellar cortex are sufficient to support sub-second timing. However, supra-second timing seems to require cortical and basal ganglia networks, perhaps operating in concert with Cerebellum.Additionally, sensory information such as an unexpected stimulus can be forwarded to the cerebellum via the climbing fiber system, providing a temporally constrained mechanism to adjust on-going behavior and modify future processing. Patients with cerebellar disorders exhibit impairments on a range of tasks that require precise timing, and recent evidence suggest that timing problems observed in other neurological conditions such as Parkinson's disease, essential tremor, and dystonia, may reflect disrupted interactions between the basal ganglia and cerebellum.The complex concepts emerging from this consensus paper should provide a foundation for further discussion, helping identify basic research questions required to understand how the brain represents and utilizes time, as well as delineating ways in which this knowledge can help improve the lives of those with neurological conditions that disrupt this most elemental sense. The panel of experts agrees that timing control in the brain is a complex concept in whom cerebellar circuitry is deeply involved. The concept of a timing machine has now expanded to clinical disorders. The Cerebellum Represents Isolated Temporal Intervals Across Task Domains Assaf Breska and Richard B. IvryIt is widely accepted that the cerebellum contributes, in some manner, to temporal processing, but the functional domain and computational mechanisms remain the subject of considerable debate. An early hypothesis was that the cerebellum served as a centralized, dedicated timing system [6,7].

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Adaptation of feedforward movement control is abnormal in patients with cervical dystonia and tremor

Cited by 27 publications

References 43 publications

Network localization of cervical dystonia based on causal brain lesions

Network localization of cervical dystonia based on causal brain lesions

Abnormal sensory gating in patients with different types of focal dystonias

Consensus paper: Decoding the Contributions of the Cerebellum as a Time Machine. From Neurons to Clinical Applications

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