Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremor
Tremor is thought to be an effect of oscillatory activity within the sensorimotor network. To date, the underlying pathological brain networks are not fully understood. Disentangling tremor activity from voluntary motor output and sensorimotor feedback systems is challenging. To better understand th...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-11-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922006693 |
| _version_ | 1818486920607432704 |
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| author | S. Sharifi F. Luft L. de Boer A.W.G. Buijink W. Mugge A.C. Schouten T. Heida L.J. Bour A.F. van Rootselaar |
| author_facet | S. Sharifi F. Luft L. de Boer A.W.G. Buijink W. Mugge A.C. Schouten T. Heida L.J. Bour A.F. van Rootselaar |
| author_sort | S. Sharifi |
| collection | DOAJ |
| description | Tremor is thought to be an effect of oscillatory activity within the sensorimotor network. To date, the underlying pathological brain networks are not fully understood. Disentangling tremor activity from voluntary motor output and sensorimotor feedback systems is challenging. To better understand the intrinsic sensorimotor fingerprint underlying tremor, we aimed to disentangle the sensorimotor system into driving (motor) and feedback/compensatory (sensory) neuronal involvement, and aimed to pinpoint tremor activity in essential tremor (ET) and tremor-dominant Parkinson's disease (PD) with a novel closed-loop approach.Eighteen ET patients, 14 tremor-dominant PD patients, and 18 healthy controls were included. An MR-compatible wrist manipulator was employed during functional MRI (fMRI) while muscle activity during (in)voluntary movements was concurrently recorded using electromyography (EMG). Tremor was quantified based on EMG and correlated to brain activity. Participants performed three tasks: an active wrist motor task, a passive wrist movement task, and rest (no wrist movement).The results in healthy controls proved that our experimental paradigm activated the expected motor and sensory networks separately using the active (motor) and passive (sensory) task. ET patients showed similar patterns of activation within the motor and sensory networks. PD patients had less activity during the active motor task in the cerebellum and basal ganglia compared to ET and healthy controls. EMG showed that in ET, tremor fluctuations correlated positively with activity in the inferior olive region, and that in PD tremor fluctuations correlated positively with cerebellar activity.Our novel approach with an MR-compatible wrist manipulator, allowed to investigate the involvement of the motor and sensory networks separately, and as such to better understand tremor pathophysiology. In ET sensorimotor network function did not differ from healthy controls. PD showed less motor-related activity. Focusing on tremor, our results indicate involvement of the inferior olive in ET tremor modulation, and cerebellar involvement in PD tremor modulation. |
| first_indexed | 2024-12-10T16:29:39Z |
| format | Article |
| id | doaj.art-dd58595f51eb4ddbafc1dfe0a0a25b12 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-10T16:29:39Z |
| publishDate | 2022-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-dd58595f51eb4ddbafc1dfe0a0a25b122022-12-22T01:41:34ZengElsevierNeuroImage1095-95722022-11-01262119554Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremorS. Sharifi0F. Luft1L. de Boer2A.W.G. Buijink3W. Mugge4A.C. Schouten5T. Heida6L.J. Bour7A.F. van Rootselaar8Department of Neurology and Clinical Neurophysiology, Amsterdam UMC, Amsterdam Neuroscience, University of Amsterdam, Meibergdreef 9, D2-113, P.O. Box 22660, Amsterdam 1100 DD, the Netherlands; BIC Brain Imaging Center, Academic Medical Center, Amsterdam, the Netherlands; Corresponding author at: Department of Neurology and Clinical Neurophysiology, Amsterdam UMC, Amsterdam Neuroscience, University of Amsterdam, Meibergdreef 9, D2-113, P.O. Box 22660, Amsterdam 1100 DD, the Netherlands.Department of Biomedical Signals and Systems, TechMed Centre, University of Twente, Enschede, the Netherlands; BIC Brain Imaging Center, Academic Medical Center, Amsterdam, the NetherlandsDepartment of Neurology and Clinical Neurophysiology, Amsterdam UMC, Amsterdam Neuroscience, University of Amsterdam, Meibergdreef 9, D2-113, P.O. Box 22660, Amsterdam 1100 DD, the NetherlandsDepartment of Neurology and Clinical Neurophysiology, Amsterdam UMC, Amsterdam Neuroscience, University of Amsterdam, Meibergdreef 9, D2-113, P.O. Box 22660, Amsterdam 1100 DD, the Netherlands; BIC Brain Imaging Center, Academic Medical Center, Amsterdam, the NetherlandsFaculty of Mechanical, Maritime and Materials Engineering, Department of Biomechanical Engineering, Delft University of Technology, Delft, the NetherlandsFaculty of Mechanical, Maritime and Materials Engineering, Department of Biomechanical Engineering, Delft University of Technology, Delft, the NetherlandsDepartment of Biomedical Signals and Systems, TechMed Centre, University of Twente, Enschede, the NetherlandsDepartment of Neurology and Clinical Neurophysiology, Amsterdam UMC, Amsterdam Neuroscience, University of Amsterdam, Meibergdreef 9, D2-113, P.O. Box 22660, Amsterdam 1100 DD, the NetherlandsDepartment of Neurology and Clinical Neurophysiology, Amsterdam UMC, Amsterdam Neuroscience, University of Amsterdam, Meibergdreef 9, D2-113, P.O. Box 22660, Amsterdam 1100 DD, the Netherlands; BIC Brain Imaging Center, Academic Medical Center, Amsterdam, the NetherlandsTremor is thought to be an effect of oscillatory activity within the sensorimotor network. To date, the underlying pathological brain networks are not fully understood. Disentangling tremor activity from voluntary motor output and sensorimotor feedback systems is challenging. To better understand the intrinsic sensorimotor fingerprint underlying tremor, we aimed to disentangle the sensorimotor system into driving (motor) and feedback/compensatory (sensory) neuronal involvement, and aimed to pinpoint tremor activity in essential tremor (ET) and tremor-dominant Parkinson's disease (PD) with a novel closed-loop approach.Eighteen ET patients, 14 tremor-dominant PD patients, and 18 healthy controls were included. An MR-compatible wrist manipulator was employed during functional MRI (fMRI) while muscle activity during (in)voluntary movements was concurrently recorded using electromyography (EMG). Tremor was quantified based on EMG and correlated to brain activity. Participants performed three tasks: an active wrist motor task, a passive wrist movement task, and rest (no wrist movement).The results in healthy controls proved that our experimental paradigm activated the expected motor and sensory networks separately using the active (motor) and passive (sensory) task. ET patients showed similar patterns of activation within the motor and sensory networks. PD patients had less activity during the active motor task in the cerebellum and basal ganglia compared to ET and healthy controls. EMG showed that in ET, tremor fluctuations correlated positively with activity in the inferior olive region, and that in PD tremor fluctuations correlated positively with cerebellar activity.Our novel approach with an MR-compatible wrist manipulator, allowed to investigate the involvement of the motor and sensory networks separately, and as such to better understand tremor pathophysiology. In ET sensorimotor network function did not differ from healthy controls. PD showed less motor-related activity. Focusing on tremor, our results indicate involvement of the inferior olive in ET tremor modulation, and cerebellar involvement in PD tremor modulation.http://www.sciencedirect.com/science/article/pii/S1053811922006693Essential tremorParkinson's diseaseTremorSensorimotor areasfMRIClosed-loop system |
| spellingShingle | S. Sharifi F. Luft L. de Boer A.W.G. Buijink W. Mugge A.C. Schouten T. Heida L.J. Bour A.F. van Rootselaar Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremor NeuroImage Essential tremor Parkinson's disease Tremor Sensorimotor areas fMRI Closed-loop system |
| title | Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremor |
| title_full | Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremor |
| title_fullStr | Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremor |
| title_full_unstemmed | Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremor |
| title_short | Closing the loop: Novel quantitative fMRI approach for manipulation of the sensorimotor loop in tremor |
| title_sort | closing the loop novel quantitative fmri approach for manipulation of the sensorimotor loop in tremor |
| topic | Essential tremor Parkinson's disease Tremor Sensorimotor areas fMRI Closed-loop system |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922006693 |
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