Top-down alteration of functional connectivity within the sensorimotor network in focal dystonia

Battistella, Giovanni; Simonyan, Kristina

doi:10.1212/wnl.0000000000007317

Cited by 65 publications

(67 citation statements)

References 41 publications

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“…In conclusion, this study is among the first to our knowledge to demonstrate common and distinct functional and structural brain abnormalities in patients with voice tremor disorders, ETv and DTv. Combined with previous studies in DTv and LD, 12,13 our findings point to the presence of a spectrum of clinical and pathophysiological characteristics across these disorders, favoring a more heterogeneous rather than dichotomous diagnostic classification of ETv and DTv. Ultimately, a refined characterization of disorder-specific abnormalities at distinct pathophysiological levels will aid the objective differential diagnosis of these disorders and help future identification of specific therapeutic targets for patients with various forms of voice tremor.…”

Section: Discussionsupporting

confidence: 77%

Neural Representations of the Voice Tremor Spectrum

Xavier

Simonyan

2020

Movement Disorders

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A BS TRACT: Objectives: Voice tremor is a common movement disorder that manifests as involuntary oscillations of laryngeal muscles, leading to rhythmic alterations in voice pitch and loudness. Differential diagnosis of essential tremor of voice (ETv) is often challenging and includes dystonic tremor of voice (DTv), which is characterized by irregular, isometric contractions of laryngeal muscles during dystonic activity. Although clinical characteristics of voice tremor are well described, the pathophysiology underlying its heterogeneous phenomenology remains limited. Methods: We used a multimodal approach of functional magnetic resonance imaging for assessment of brain activity during symptomatic speech production, highresolution magnetic resonance imaging for the examination of cortical thickness and gray matter volume, and diffusion-weighted imaging for evaluation of white matter integrity to identify disorder-specific neural alterations and their relationships with the symptomatology of ETv and DTv. Results: We found a broad overlap between cortical alterations in ETv and DTv, involving sensorimotor regions responsible for the integration of multisensory information during speech production, such as primary sensorimotor, inferior/superior parietal, and inferior temporal cortices. In addition, ETv and DTv showed unique patterns of abnormalities in regions controlling speech motor preparation, which were localized in the cerebellum in ETv and the premotor cortex, insula, and superior temporal gyrus in DTv. Neural alterations in superior parietal and inferior temporal cortices were correlated with ETv severity, whereas changes in the left premotor cortex were associated with DTv severity. Conclusions: Our findings point to the pathophysiological spectrum underlying ETv and DTv and favor a more heterogeneous rather than dichotomous diagnostic classification of these voice tremor disorders.

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Section: Discussionsupporting

confidence: 77%

Neural Representations of the Voice Tremor Spectrum

Xavier

Simonyan

2020

Movement Disorders

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“…Other rs-fMRI studies in spasmodic dysphonia described reduced connectivity in either the supplementary motor area or the PMd within the SMN. Yet, cluster locations differed compared to the present study, and the lack of dimensionality information in previous studies impairs comparability 8,36 . Disordered information transfer from the sensory to the motor cortices (i.e sensorimotor integration) is discussed as a possible mechanism of dystonic posturing 17 , occurring either at the cortico-cortical or subcortico-cortical level involving the basal ganglia or cerebellum 37,38 .…”

Section: Discussioncontrasting

confidence: 70%

“…Disordered information transfer from the sensory to the motor cortices (i.e sensorimotor integration) is discussed as a possible mechanism of dystonic posturing 17 , occurring either at the cortico-cortical or subcortico-cortical level involving the basal ganglia or cerebellum 37,38 . In support of a possible top-down process (from those cortices to primary/subcortical areas), recent work in spasmodic dysphonia suggested abnormal premotor-parietal-putaminal circuitry with abnormal excitatory left inferior parietal projections to the putamen and interhemispheric information transfer from the right to left premotor cortex 36 . Yet, the lack of differentiability of primary and adaptive changes by fMRI ultimately limited the interpretation of the findings' origins.…”

Section: Discussionmentioning

confidence: 99%

Altered sensory system activity and connectivity patterns in adductor spasmodic dysphonia

Mantel

Dresel

Welte

et al. 2020

Sci Rep

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Adductor-type spasmodic dysphonia (ADSD) manifests in effortful speech temporarily relievable by botulinum neurotoxin type A (Bont-A). previously, abnormal structure, phonation-related and resting-state sensorimotor abnormalities as well as peripheral tactile thresholds in ADSD were described. this study aimed at assessing abnormal central tactile processing patterns, their spatial relation with dysfunctional resting-state connectivity, and their Bont-A responsiveness. functional MRI in 14/12 ADSD patients before/under BoNT-A effect and 15 controls was performed (i) during automatized tactile stimulus application to face/hand, and (ii) at rest. Between-group differential stimulation-induced activation and resting-state connectivity (regional homogeneity, connectivity strength within selected sensory(motor) networks), as well as within-patient BoNT-A effects on these differences were investigated. Contralateral-to-stimulation overactivity in ADSD before BoNT-A involved primary and secondary somatosensory representations, along with abnormalities in higherorder parietal, insular, temporal or premotor cortices. Dysphonic impairment in ADSD positively associated with left-hemispheric temporal activity. connectivity was increased within right premotor (sensorimotor network), left primary auditory cortex (auditory network), and regionally reduced at the temporoparietal junction. Activation/connectivity before/after BoNT-A within-patients did not significantly differ. Abnormal ADSD central somatosensory processing supports its significance as common pathophysiologic focal dystonia trait. Abnormal temporal cortex tactile processing and resting-state connectivity might hint at abnormal cross-modal sensory interactions.

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“…Taking into account these findings in healthy individuals, the correlations between temporal discrimination and inferior parietal activity as well as any other brain regions present in healthy individuals were lost in nonmusician's dystonia, likely leading to abnormally increased TDT in these patients. Abnormal structural organization, functional activity, and connectivity of the inferior parietal cortex, including the angular gyrus, have been increasingly implicated in the pathophysiology of focal hand dystonia and laryngeal dystonia . Vulnerable parietal–premotor functional connectivity has been associated with the polygenic risk of dystonia, whereas maladaptive plasticity of the inferior parietal cortex has been related to the loss of inhibition as a result of reduced gamma‐aminobutyric acid (GABA)‐ergic function .…”

Section: Discussionmentioning

confidence: 99%

Normal Temporal Discrimination in Musician's Dystonia Is Linked to Aberrant Sensorimotor Processing

2020

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A BS TRACT: Objectives: Alterations in sensory discrimination are a prominent nonmotor feature of dystonia. Abnormal temporal discrimination in focal dystonia is considered to represent its mediational endophenotype, albeit unclear pathophysiological correlates. We examined the associations between the visual temporal discrimination threshold (TDT) and brain activity in patients with musician's dystonia, nonmusician's dystonia, and healthy controls. Methods: A total of 42 patients and 41 healthy controls participated in the study. Between-group differences in TDT z scores were computed using inferential statistics. Statistical associations of TDT z scores with clinical characteristics of dystonia and resting-state functional brain activity were examined using nonparametric rank correlations. Results: The TDT z scores of healthy controls were significantly different from those of patients with nonmusician's dystonia, but not of patients with musician's dystonia. Healthy controls showed a significant relationship between normal TDT levels and activity in the inferior parietal cortex. This relationship was lost in all patients. Instead, TDT z scores in musician's dystonia established additional correlations with activity in premotor, primary somatosensory, ventral extrastriate cortices, inferior occipital gyrus, precuneus, and cerebellum, whereas nonmusician's dystonia showed a trending correlation in the lingual gyrus extending to the cerebellar vermis. There were no significant relationships between TDT z scores and dystonia onset, duration, or severity. Conclusions: TDT assessment as an endophenotypic marker may only be relevant to nonmusician forms of dystonia because of the lack of apparent alterations in musician's dystonia. Compensatory adaptation of neural circuitry responsible for TDT processing likely adjusted the TDT performance to the behaviorally normal levels in patients with musician's dystonia, but not nonmusician's dystonia.

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Top-down alteration of functional connectivity within the sensorimotor network in focal dystonia

Cited by 65 publications

References 41 publications

Neural Representations of the Voice Tremor Spectrum

Neural Representations of the Voice Tremor Spectrum

Altered sensory system activity and connectivity patterns in adductor spasmodic dysphonia

Normal Temporal Discrimination in Musician's Dystonia Is Linked to Aberrant Sensorimotor Processing

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