Deep brain stimulation in the caudal zona incerta modulates the sensorimotor cerebello-cerebral circuit in essential tremor

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Awad, AmarUmeå universitet,Umeå centrum för funktionell hjärnavbildning (UFBI),Institutionen för integrativ medicinsk biologi (IMB) (author)

Deep brain stimulation in the caudal zona incerta modulates the sensorimotor cerebello-cerebral circuit in essential tremor

Article/chapterEnglish2020

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Elsevier,2020
electronicrdacarrier

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LIBRIS-ID:oai:DiVA.org:umu-167200
https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-167200URI
https://doi.org/10.1016/j.neuroimage.2019.116511DOI

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Language:English
Summary in:English

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Subject category:art swepub-publicationtype

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Essential tremor is effectively treated with deep brain stimulation (DBS), but the neural mechanisms underlying the treatment effect are poorly understood. Essential tremor is driven by a dysfunctional cerebello-thalamo-cerebral circuit resulting in pathological tremor oscillations. DBS is hypothesised to interfere with these oscillations at the stimulated target level, but it is unknown whether the stimulation modulates the activity of the cerebello-thalamo-cerebral circuit during different task states (with and without tremor) in awake essential tremor patients. To address this issue, we used functional MRI in 16 essential tremor patients chronically implanted with DBS in the caudal zona incerta. During scanning, the patients performed unilateral tremor-inducing postural holding and pointing tasks as well as rest, with contralateral stimulation turned On and Off.We show that DBS exerts both task-dependent as well as task-independent modulation of the sensorimotor cerebello-cerebral regions (p ≤ 0.05, FWE cluster-corrected for multiple comparisons). Task-dependent modulation (DBS × task interaction) resulted in two patterns of stimulation effects. Firstly, activity decreases (blood oxygen level-dependent signal) during tremor-inducing postural holding in the primary sensorimotor cortex and cerebellar lobule VIII, and activity increases in the supplementary motor area and cerebellar lobule V during rest (p ≤ 0.05, post hoc two-tailed t-test). These effects represent differences at the effector level and may reflect DBS-induced tremor reduction since the primary sensorimotor cortex, cerebellum and supplementary motor area exhibit less motor task-activity as compared to the resting condition during On stimulation. Secondly, task-independent modulation (main effect of DBS) was observed as activity increase in the lateral premotor cortex during all motor tasks, and also during rest (p ≤ 0.05, post hoc two-tailed t-test). This task-independent effect may mediate the therapeutic effects of DBS through the facilitation of the premotor control over the sensorimotor circuit, making it less susceptible to tremor entrainment.Our findings support the notion that DBS in essential tremor is modulating the sensorimotor cerebello-cerebral circuit, distant to the stimulated target, and illustrate the complexity of stimulation mechanisms by demonstrating task-dependent as well as task-independent actions in cerebello-cerebral regions.

Subject headings and genre

MEDICIN OCH HÄLSOVETENSKAP Klinisk medicin Neurologi hsv//swe
MEDICAL AND HEALTH SCIENCES Clinical Medicine Neurology hsv//eng
MEDICIN OCH HÄLSOVETENSKAP Medicinska och farmaceutiska grundvetenskaper Fysiologi hsv//swe
MEDICAL AND HEALTH SCIENCES Basic Medicine Physiology hsv//eng
MEDICIN OCH HÄLSOVETENSKAP Medicinska och farmaceutiska grundvetenskaper Neurovetenskaper hsv//swe
MEDICAL AND HEALTH SCIENCES Basic Medicine Neurosciences hsv//eng
Essential tremor
Deep brain stimulation
Caudal zona incerta
Functional MRI
Cerebello-cerebral circuit
neurokirurgi
Neurosurgery
Neurology
neurologi
Physiology
fysiologi

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Blomstedt, PatricUmeå universitet,Klinisk neurovetenskap(Swepub:umu)pabl0002 (author)
Westling, GöranUmeå universitet,Institutionen för integrativ medicinsk biologi (IMB)(Swepub:umu)gorweg00 (author)
Eriksson, JohanUmeå universitet,Umeå centrum för funktionell hjärnavbildning (UFBI),Institutionen för integrativ medicinsk biologi (IMB)(Swepub:umu)joer0003 (author)
Umeå universitetUmeå centrum för funktionell hjärnavbildning (UFBI) (creator_code:org_t)

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In:NeuroImage: Elsevier2091053-81191095-9572

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