Movement-induced uncoupling of primary sensory and motor areas in focal task-specific hand dystonia
•Through an ad hoc procedure (FSS), distinct sources were identified in S1 and M1.•No differences were found between spectral properties of patients and controls for either S1 and M1.•Gamma band S1–M1 coherence was bilaterally reduced in patients during movement.•In focal hand dystonia, uncoupling r...
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| Veröffentlicht in: | Neuroscience Jg. 250; S. 434 - 445 |
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10.10.2013
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| ISSN: | 0306-4522, 1873-7544, 1873-7544 |
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| Abstract | •Through an ad hoc procedure (FSS), distinct sources were identified in S1 and M1.•No differences were found between spectral properties of patients and controls for either S1 and M1.•Gamma band S1–M1 coherence was bilaterally reduced in patients during movement.•In focal hand dystonia, uncoupling replaces the physiological sensorimotor coupling.•Bi-hemispheric abnormalities in unilateral dystonia suggest endophenotypic traits.
Due to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1) and primary motor (M1) cortex source activities and their functional cross-talk during a non-dystonia-inducing sensorimotor task free of biases generated by the interfering with the occurrence of dystonic movements.
Magnetoencephalographic brain signals and opponens pollicis (OP) electromyographic activities were acquired at rest and during a simple isometric contraction performed either alone or in combination with median nerve stimulation. The task was performed separately with the right and left hand by eight patients suffering from focal task-specific hand dystonia and by eight healthy volunteers. Through an ad hoc procedure Functional Source Separation (FSS), distinct sources were identified in S1 (FSS1) and M1 (FSM1) devoted to hand control. Spectral properties and functional coupling (coherence) between the two sources were assessed in alpha [8,13]Hz, beta [14,32]Hz and gamma [33,45]Hz frequency bands.
No differences were found between spectral properties of patients and controls for either FSM1 or FSS1 cerebral sources. Functional coupling between FSM1 and FSS1 (gamma band coherence), while comparable between dystonic patients and healthy controls at rest, was selectively reduced in patients during movement. All findings were present in both hemispheres.
Because previous literature has shown that gamma-band sensory–motor synchronization reflects an efficiency index of sensory–motor integration, our data demonstrate that, in dystonic patients, uncoupling replaces the functional coupling required for efficient sensory–motor control during motor exertion. The presence of bi-hemispheric abnormalities in unilateral hand dystonia supports the presence of an endophenotypic trait. |
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| AbstractList | Introduction Due to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1) and primary motor (M1) cortex source activities and their functional cross-talk during a non-dystonia-inducing sensorimotor task free of biases generated by the interfering with the occurrence of dystonic movements. Method Magnetoencephalographic brain signals and opponens pollicis (OP) electromyographic activities were acquired at rest and during a simple isometric contraction performed either alone or in combination with median nerve stimulation. The task was performed separately with the right and left hand by eight patients suffering from focal task-specific hand dystonia and by eight healthy volunteers. Through an ad hoc procedure Functional Source Separation (FSS), distinct sources were identified in S1 (FSS1) and M1 (FSM1) devoted to hand control. Spectral properties and functional coupling (coherence) between the two sources were assessed in alpha [8,13]Hz, beta [14,32]Hz and gamma [33,45]Hz frequency bands. Results No differences were found between spectral properties of patients and controls for either FSM1 or FSS1 cerebral sources. Functional coupling between FSM1 and FSS1 (gamma band coherence), while comparable between dystonic patients and healthy controls at rest, was selectively reduced in patients during movement. All findings were present in both hemispheres. Discussion Because previous literature has shown that gamma-band sensory-motor synchronization reflects an efficiency index of sensory-motor integration, our data demonstrate that, in dystonic patients, uncoupling replaces the functional coupling required for efficient sensory-motor control during motor exertion. The presence of bi-hemispheric abnormalities in unilateral hand dystonia supports the presence of an endophenotypic trait. Due to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1) and primary motor (M1) cortex source activities and their functional cross-talk during a non-dystonia-inducing sensorimotor task free of biases generated by the interfering with the occurrence of dystonic movements.INTRODUCTIONDue to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1) and primary motor (M1) cortex source activities and their functional cross-talk during a non-dystonia-inducing sensorimotor task free of biases generated by the interfering with the occurrence of dystonic movements.Magnetoencephalographic brain signals and opponens pollicis (OP) electromyographic activities were acquired at rest and during a simple isometric contraction performed either alone or in combination with median nerve stimulation. The task was performed separately with the right and left hand by eight patients suffering from focal task-specific hand dystonia and by eight healthy volunteers. Through an ad hoc procedure Functional Source Separation (FSS), distinct sources were identified in S1 (FSS1) and M1 (FSM1) devoted to hand control. Spectral properties and functional coupling (coherence) between the two sources were assessed in alpha [8,13]Hz, beta [14,32]Hz and gamma [33,45]Hz frequency bands.METHODMagnetoencephalographic brain signals and opponens pollicis (OP) electromyographic activities were acquired at rest and during a simple isometric contraction performed either alone or in combination with median nerve stimulation. The task was performed separately with the right and left hand by eight patients suffering from focal task-specific hand dystonia and by eight healthy volunteers. Through an ad hoc procedure Functional Source Separation (FSS), distinct sources were identified in S1 (FSS1) and M1 (FSM1) devoted to hand control. Spectral properties and functional coupling (coherence) between the two sources were assessed in alpha [8,13]Hz, beta [14,32]Hz and gamma [33,45]Hz frequency bands.No differences were found between spectral properties of patients and controls for either FSM1 or FSS1 cerebral sources. Functional coupling between FSM1 and FSS1 (gamma band coherence), while comparable between dystonic patients and healthy controls at rest, was selectively reduced in patients during movement. All findings were present in both hemispheres.RESULTSNo differences were found between spectral properties of patients and controls for either FSM1 or FSS1 cerebral sources. Functional coupling between FSM1 and FSS1 (gamma band coherence), while comparable between dystonic patients and healthy controls at rest, was selectively reduced in patients during movement. All findings were present in both hemispheres.Because previous literature has shown that gamma-band sensory-motor synchronization reflects an efficiency index of sensory-motor integration, our data demonstrate that, in dystonic patients, uncoupling replaces the functional coupling required for efficient sensory-motor control during motor exertion. The presence of bi-hemispheric abnormalities in unilateral hand dystonia supports the presence of an endophenotypic trait.DISCUSSIONBecause previous literature has shown that gamma-band sensory-motor synchronization reflects an efficiency index of sensory-motor integration, our data demonstrate that, in dystonic patients, uncoupling replaces the functional coupling required for efficient sensory-motor control during motor exertion. The presence of bi-hemispheric abnormalities in unilateral hand dystonia supports the presence of an endophenotypic trait. Due to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1) and primary motor (M1) cortex source activities and their functional cross-talk during a non-dystonia-inducing sensorimotor task free of biases generated by the interfering with the occurrence of dystonic movements. Magnetoencephalographic brain signals and opponens pollicis (OP) electromyographic activities were acquired at rest and during a simple isometric contraction performed either alone or in combination with median nerve stimulation. The task was performed separately with the right and left hand by eight patients suffering from focal task-specific hand dystonia and by eight healthy volunteers. Through an ad hoc procedure Functional Source Separation (FSS), distinct sources were identified in S1 (FSS1) and M1 (FSM1) devoted to hand control. Spectral properties and functional coupling (coherence) between the two sources were assessed in alpha [8,13]Hz, beta [14,32]Hz and gamma [33,45]Hz frequency bands. No differences were found between spectral properties of patients and controls for either FSM1 or FSS1 cerebral sources. Functional coupling between FSM1 and FSS1 (gamma band coherence), while comparable between dystonic patients and healthy controls at rest, was selectively reduced in patients during movement. All findings were present in both hemispheres. Because previous literature has shown that gamma-band sensory-motor synchronization reflects an efficiency index of sensory-motor integration, our data demonstrate that, in dystonic patients, uncoupling replaces the functional coupling required for efficient sensory-motor control during motor exertion. The presence of bi-hemispheric abnormalities in unilateral hand dystonia supports the presence of an endophenotypic trait. •Through an ad hoc procedure (FSS), distinct sources were identified in S1 and M1.•No differences were found between spectral properties of patients and controls for either S1 and M1.•Gamma band S1–M1 coherence was bilaterally reduced in patients during movement.•In focal hand dystonia, uncoupling replaces the physiological sensorimotor coupling.•Bi-hemispheric abnormalities in unilateral dystonia suggest endophenotypic traits. Due to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1) and primary motor (M1) cortex source activities and their functional cross-talk during a non-dystonia-inducing sensorimotor task free of biases generated by the interfering with the occurrence of dystonic movements. Magnetoencephalographic brain signals and opponens pollicis (OP) electromyographic activities were acquired at rest and during a simple isometric contraction performed either alone or in combination with median nerve stimulation. The task was performed separately with the right and left hand by eight patients suffering from focal task-specific hand dystonia and by eight healthy volunteers. Through an ad hoc procedure Functional Source Separation (FSS), distinct sources were identified in S1 (FSS1) and M1 (FSM1) devoted to hand control. Spectral properties and functional coupling (coherence) between the two sources were assessed in alpha [8,13]Hz, beta [14,32]Hz and gamma [33,45]Hz frequency bands. No differences were found between spectral properties of patients and controls for either FSM1 or FSS1 cerebral sources. Functional coupling between FSM1 and FSS1 (gamma band coherence), while comparable between dystonic patients and healthy controls at rest, was selectively reduced in patients during movement. All findings were present in both hemispheres. Because previous literature has shown that gamma-band sensory–motor synchronization reflects an efficiency index of sensory–motor integration, our data demonstrate that, in dystonic patients, uncoupling replaces the functional coupling required for efficient sensory–motor control during motor exertion. The presence of bi-hemispheric abnormalities in unilateral hand dystonia supports the presence of an endophenotypic trait. Highlights • Through an ad hoc procedure (FSS), distinct sources were identified in S1 and M1. • No differences were found between spectral properties of patients and controls for either S1 and M1. • Gamma band S1–M1 coherence was bilaterally reduced in patients during movement. • In focal hand dystonia, uncoupling replaces the physiological sensorimotor coupling. • Bi-hemispheric abnormalities in unilateral dystonia suggest endophenotypic traits. |
| Author | Tomasevic, L. Tecchio, F. Melgari, J.M. Rossini, P.M. Zappasodi, F. Porcaro, C. Cassetta, E. |
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| Keywords | PSD focal task-specific hand dystonia OP M1 coherence ICA ECD FSS FSS1 contra-D FS MEG sensorimotor integration FSM1 functional connectivity ANOVA magnetoencephalography (MEG) ipsi-D S1 Functional Source Separation primary sensory cortex Independent Component Analysis functional source hemisphere ipsilateral to the dystonic arm equivalent current dipole analysis of variance opponens pollicis primary motor cortex hand primary motor cortex Functional Source hand primary sensory cortex Functional Source Power Spectral Density FS S1 hemisphere contralateral to the dystonic arm FS M1 magnetoencephalography Sensorimotor coordination Magnetoencephalography Hand FS(S1) FS(M1) |
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| Snippet | •Through an ad hoc procedure (FSS), distinct sources were identified in S1 and M1.•No differences were found between spectral properties of patients and... Highlights • Through an ad hoc procedure (FSS), distinct sources were identified in S1 and M1. • No differences were found between spectral properties of... Due to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1) and primary... Introduction Due to growing evidence of sensorimotor integration impairment in focal task-specific hand dystonia, we aimed at describing primary sensory (S1)... |
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| SubjectTerms | Adult Biological and medical sciences coherence Data Interpretation, Statistical Dystonia - physiopathology Dystonic Disorders - physiopathology Electric Stimulation Electroencephalography Electroencephalography Phase Synchronization Female focal task-specific hand dystonia functional connectivity Functional Source Separation Fundamental and applied biological sciences. Psychology Hand Humans Magnetoencephalography magnetoencephalography (MEG) Male Middle Aged Motor Cortex - physiology Movement - physiology Muscle Contraction - physiology Muscle Relaxation - physiology Neurology sensorimotor integration Somatosensory Cortex - physiopathology Vertebrates: nervous system and sense organs |
| Title | Movement-induced uncoupling of primary sensory and motor areas in focal task-specific hand dystonia |
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