Abnormal subcortical activity in congenital mirror movement disorder with RAD51 mutation.
The etiology of abnormal mirror movements is diverse, including central nervous system disorders such as Klippel-Feil syndrome (6, 7), X-linked Kallman syndrome (8), ischemic stroke (9), and hemiplegic cerebral palsy (10). Unlike the aforementioned central nervous system disorders, congenital mirror movement disorder (CMMD) is characterized by persistent mirror movements with no other neurologic abnormalities (11). Genetic origin of CMMD may be familial or sporadic. Familial CMMD usually has an autosomal dominant inheritance pattern (12, 13). RAD51 haploinsufficiency causes CMMD in humans (14). RAD51 gene plays a critical role in healthy motor system development. It has a focal expression at the pyramidal decussation during critical neurodevelopmental stages. RAD51 expression was detected in corticospinal axons at the pyramidal decussation in two-day-old mouse models and its deficiency specifically alters the development of an intact de-cussation tract (14). Results of other studies on affected human individuals suggest that heterozygous mutations in DCC gene also causes CMMD (15). The DCC gene is a receptor protein for netrin, which is involved in axonal migration of neurons across the body's midline during the developmental stage (16). Abnormalities in axon guidance and the corticospinal tract (CST) are observed in the absence of ephrin or DCC genes in knock-out animal studies (17, 18).
As we have discussed previously, abnormal cortical activity accompanies the mirror movements in CMMD (19, 20). However, the motor loop contains not only cortical areas, but also subcortical structures. Subcortical components of the motor system, including basal ganglia and cerebellum, provide effective control mechanisms. Thalamus is another key player for the information flow: it receives projections from the subcortical nuclei and projects onto the cerebral cortex (21). These structures are critical to initiate, gate and terminate motor movements, but their roles in mirror movement disorder remain unknown. To address this knowledge gap in literature, using functional magnetic resonance imaging (fMRI), we investigated task-related brain activity, including that in thalamus and basal ganglia, in two CMMD patients with RAD51 mutations and matched healthy participants.
Two brothers (aged, 29 and 30 years) exhibiting familial CMMD on the distal upper limbs were studied in task-based fMRI scans (see Supplementary Fig. 1). The patients were from a Turkish family with seven effected members. For the genetic assessments three generations of the family were examined, which revealed a RAD51 deleterious mutation (see Supplementary Figs. 2-4). All affected individuals of the family exhibit mirror movements in hands, fingers, and forearms with onset in infancy without any associated neurologic abnormalities. Also, there were no structural abnormalities including infarction on their structural T1-weighted images. Ten age and sex-matched healthy participants (mean age, 30.9[+ or -]5.04 years) were included as a control group.
Neurologic examinations of the patients were conducted by neurologists who were experienced on electrophysiology and movement disorders in our group. Severity of CMMD was rated by Wood-Teuber scale (0, no mirror movement; 1, hardly perceivable with repetitive mirror movement; 2, barely discernible with sustained mirror movement or obvious with brief-periodic mirror movements; 3, obvious and sustained repetitive mirror movement; 4, strong mirror movement activity in unintended side). Our patients were rated 3 in mirror movement scale with no mental retardation, normal speech and walking skills.
Informed written consent was obtained from all participants in accordance with the declaration of Helsinki and procedures and protocols were approved by the Institutional Human Subjects Ethics Committee (Approval Number:2010_08_32_2).
fMRI data acquisition
MRI data were acquired in a Siemens 3T MAGNETOM Trio scanner fitted with a 12-channel phase-array head-coil. High resolution T1-weighted three-dimensional MPRAGE images were acquired in each session (single shot turbo flash; voxel size, 1X1X1 [mm.sup3]; repetition time [TR], 2600 ms; echo time [TE], 3.02 ms; flip angle, 8 degrees; field of view [FOV], 256 X 224 [mm.sup.2]; slice orientation, sagittal; phase encode direction, anterior-posterior; number of slices, 176; acceleration factor (GRAPPA), 2). For the functional scans an echo-planar imaging (EPI) sequence was used (voxel size, 3X3X3 [mm.sup.3]; TR, 2000 ms; TE, 40 ms; flip angle, 71 degrees; FOV, 192X192 [mm.sup2]; slice orientation, transverse; number of slices, 26). Subjects participated in two scanning sessions; each started with the structural scan, followed by the task-based functional runs.
In a block-design protocol participants performed index finger tapping movement following visually presented cues during a 12 s active block. Active blocks were repeated for five times interspersed with 12 s rest blocks. Visual stimuli were composed of a green arrow placed at the center of the stimulus display and pointed to the side of required movement (left, right and both) for the active conditions as well as a closed-end green line for the rest condition. Our group created the experimental stimulus using the Java programming platform.
Data were preprocessed using the tools in Statistical Parametric Mapping software (SPM8, http://www.fil.ion.ucl.ac.uk/spm/software/spm8/) implemented in MATLAB (Mathworks, Inc.). Preprocessing steps included image realignment, slice acquisition-time correction, and functional and anatomical image coregistration. Functional images were normalized to Montreal Neurological Institute's (MNI) template by fitting mean functional images to the single reference EPI standard SPM template, and smoothed with a 6 mm Gaussian kernel to reduce spatial noise. Next, first level statistical parameters were computed for each participant using the GLM procedure implemented in FSL fMRI Expert Analysis Tool FEAT, version 5.6.3. Contrasts of right finger movement versus rest, left finger movement versus rest, and bimanual finger movement versus rest were defined to obtain z-score maps over the whole brain. To compare control and patient groups, spherical regions of interest (ROIs) were created by using FSL in the bilateral M1s (hand area), SMA, thalamus, globus pallidus, putamen and caudate with 6 mm Gaussian kernel radius on each participants' functional data (Table 1). Putamen and caudate ROIs were combined and analyzed as striatum since they are histologically identical and both are composed of similar projection fibers (22). Then these ROIs were binarized and applied onto the z-score maps of individuals for each contrast.
The mean z-scores were analyzed by conducting a mixed design 3-way ANOVA (Group X Task side X Hemisphere) to compare activations in unimanual movements. Bilateral movements were analyzed through a mixed design 2-way ANOVA (Group X Hemisphere). Tukey's post hoc analyses were performed where appropriate. Statistical parametric maps were projected onto 3D morphed brain surface to visualize the cortex activation, and onto 2D T1-weighted images to visualize activation in subcortical structures by using BrainVoyager QX 2.8.
We measured fMRI BOLD (blood-oxygen-level-dependent) activity in thalamus, striatum, globus pallidus, supplementary motor area (SMA) and the hand area of primary motor cortex (M1) during a finger tapping task (left, right, bimanual). We summarized demographic characterization of both groups and statistical results in Table 2. Also, Figs. 1 and 2 show the statistical parametric maps on inflated cortices as well as average fMRI responses in some of the predefined ROIs. fMRI responses, more specifically the z-scores, in the ROIs were compared between the patients and controls by using mixed-design ANOVAs and Tukey's post-hoc correction where appropriate. For the bimanual movement we found no main effect of group or hemisphere in any of the areas tested. During the bimanual movement BOLD activity in predefined ROIs was not statistically different between the patient and control groups nor between right and left hemispheres. For the unimanual movements, activations of M1, thalamus, and striatum showed group main effect (M1: F(1, 10)=10.761, P = 0.008; thalamus: F(1, 10)=8.686, P = 0.015; striatum: F(1,10)=7.069, P = 0.024). Activity in M1, thalamus, and striatum was statistically different between patients and healthy controls during the unimanual movement execution. However, the activity in globus pallidus showed a marginal trend toward significance between patient group and healthy controls. In globus pallidus, group main effect during unimanual movements was observed with marginal statistical significance (globus pallidus: F(1,10)=4.893, P = 0.051). There was an interaction between hemisphere and task side in M1, thalamus, and SMA (M1: F(1, 10)=20.235, P = 0.001; thalamus: F(1, 10)=10.028, P = 0.010; SMA: F(1, 10)=5.666, P = 0.039). The interaction showed that ipsilateral motor activity was greater in patients compared with controls in M1, thalamus, and SMA areas, whereas there was less or no intergroup difference in the contralateral side during both right and left unimanual finger movements. In SMA we also found a main effect of hemisphere (F(1, 10)=6.884, P = 0.025) and interaction between hemisphere and group (F(1, 10)=9.225, P = 0.013). The activity in SMA was statistically different between left and right hemispheres during the unimanual right and left finger movements in both patient and control groups. Also, motor activity was statistically different in the left SMA between patients and control groups (i.e., mean z-score of the left SMA was always larger in controls), whereas the difference was smaller during the right finger movement or nonsignificant during the left finger movement in the right SMA (Fig. 1, Table 2).
Further group comparisons between statistically significant variables were performed by using independent samples t-test. Our analyses revealed statistically significant differences during right finger movement between groups in M1 and thalamus bilaterally and in the right striatum (Left M1: t(10)=-2.686, P = 0.023, right M1: t(10)=-4.014, P = 0.002; left thalamus: t(10)=-2.935, P = 0.015, right thalamus: t(10)=-2.495, P = 0.032; right striatum: t(10)=-3.337, P = 0.008). Critically, in M1 there was a significant difference between left and right finger movements in controls (Right M1: t(9)=-7.779, P < 0.001, left M1: t(9)=9.976, P = 0.003) but not in patients (Right M1: t(1)=-2.021, P = 0.293, left M1: t(1)=2.992, P = 0.205). Responses obtained from thalamus during unimanual movements were significantly higher in patients (Fig. 2). In globus pallidus, a similar trend was observed with marginal statistical significance (F(1,10)=4.893, P = 0.051).
In summary, our analyses revealed abnormal lateralization in M1 and SMA during unimanual movements, which is consistent with previous findings in the literature (19). Furthermore, we have also found previously unknown abnormal activation in thalamus, and in the components of basal ganglia.
We investigated task-related activity within the components of the motor system of CMMD patients with RAD51 mutation. Task-related fMRI results showed abnormal activity in M1, thalamus, striatum, globus pallidus (marginally significant) and SMA in the patients. Results highlight that execution of unilateral motor movements critically depends on the healthy interactions not only at the cortical level but also at subcortical levels.
Two main, but not mutually exclusive, hypotheses have been proposed to explain the mirror movement disorder at the nervous system level. One hypothesis posits that mirror movements occur because of abnormally uncrossed corticospinal fibers originating in primary motor cortices (M1) (23). This hypothesis is supported by the temporal characteristics of bilateral electromyography (EMG) activity during the unilateral M1 activation (24, 25), and motor evoked potentials (MEPs) in transcranial magnetic stimulation (TMS) studies (19). In the neurologic examination part of the study our TMS results replicate the findings in the literature (Supplementary Fig. 1). Thus, abnormally uncrossed corticospinal fibers could be a contributing mechanism to CMMD with RAD51 mutation.
According to the other hypothesis, abnormally reduced lateralization of activity in M1 leads to mirror movements. In healthy individuals M1 activity is largely restricted to the contralateral side of the intended unimanual movements. However, in CMMD patients there is an abnormally increased activity in M1 that is ipsilateral to the side of the intended voluntary movement, leading to a bilateral activation pattern in M1s (19, 20). The cause of this bilateral M1 activity is largely unknown. Reduced or absent interhemispheric (19) or intracortical (26) inhibition could lead to this bilateral activation pattern. For example, irregular activity of secondary motor areas, which regulate the M1 activity, could lead to the abnormal bilateral M1 activity (23). In a recent study, Gallea et al. (19) investigated CMMD patients with RAD51 haploinsufficiency by using single-pulse TMS, diffusion-weighted imaging, and fMRI techniques. In those patients abnormal decussation of CST, bilateral M1 activity during intended unimanual movements, and abnormal interhemispheric inhibition were found (19). Furthermore, effective connectivity analyses of fMRI data revealed abnormal interaction between SMA and M1 during unimanual and bimanual movements (19). In the present study, M1 activity was largely contralateral to the side of unimanual finger movements in healthy participants, whereas it was bilateral in patients. This kind of abnormal lateralization was previously observed in CMMD patients (7, 20). However, its cause is not clearly understood. It is known that the activity of M1 is regulated by other cortical and subcortical areas. For example, during a unimanual action, the activity of the M1 ipsilateral to the intended hand is temporarily suppressed (27). TMS studies also showed interhemispheric inhibitory interactions between the two M1s (28). Thus, it is possible that the abnormal ipsilateral M1 activity arises because of a lack of interhemispheric inhibition between the two M1s (19). At the cortex, SMA also showed abnormal activation pattern during unimanual movements in CMMD patients, once again consistent with previous findings (19). In normal controls left SMA activity was larger under all conditions (right, left, bimanual movements). However, in patients activity was not equally strongly lateralized to the left SMA.
Although cortical abnormalities have been well documented in the literature, and shown to be consistent with our findings, activity patterns in subcortical structures have not been studied previously, despite their critical involvement in motor movements. Our results show that activity of thalamus, a subcortical structure, was also abnormal in the CMMD patients. Overall thalamic activity was larger in patients during intended unimanual finger movements. Similarly, BOLD activity in the other subcortical structures including the components of basal ganglia, namely striatum and globus pallidus, activity was statistically different between patient and healthy control groups during unimanual finger movements (in globus pallidus statistically marginally significant). Thalamus is an important gateway for information projecting to and from the cortex, including the links to sensory organs. Thus, any abnormality in the activity of thalamus could have severe repercussions in motor actions. Likewise, basal ganglia plays a key role in sequential movements in timing and selecting the specific muscles for the execution of movement (29). Basal ganglia consist of a set of nuclei located in cerebrum and has inhibitory GABAergic projection neurons (30). When striatal projections are activated by the cortex, due to their neurochemical properties they tend to suppress the tonically active pallidal output that projects to thalamus (30). By means of this pathway, activity of the striatal neurons may lead phasic decrease of discharge of activity of pallidal neurons, which in turn disinhibits the activity of the thalamus. Outcome of this disinhibition is facilitation of the motor cortex. SMA receives strong indirect projections from the basal ganglia via the thalamus (31). Abnormal connectivity between SMA and M1, along with the increased globus pallidus, striatum, and thalamic activity during task execution in patients may lead to mirror movements through blocking the non-mirroring transformation of unilateral movement in SMA.
Our patients carry RAD51 mutation. RAD51 gene is involved in repairing DNA double stranded breaks by homologous recombination (32). In addition, it is also linked to the development of the decussation tract in the spinal cord (33). Our findings suggest that the effect of RAD51 mutation may not be limited to the organization of the decussation tract but also extend to overall organization of the motor system. The findings presented here could also be a consequence of a reorganization of the nervous system to compensate for the direct impact of the mutation during development. Longitudinal studies, including the developmental stages can help researchers resolve this confound. To better understand the biological background of the reorganization of cortical and subcortical nuclei, in vivo studies would also be needed. Functional and structural connectivity analyses between the components of the motor loop in CMMD with larger patient population may provide further information. Nevertheless, such a rare case study provides valuable information about the possible extent of the effects of RAD51 mutation on human anatomical and functional brain architecture.
There are some limitations of our study that need to be taken into account when interpreting the data. First, our patient group consists of only two individuals who have the same mutational locus. Despite the apparent uniformity of clinical features, functional effects of genetic heterogeneity of the disorder on motor circuit is not clear (33). Although we had conducted genetic analyses to a few other family members, we include only two individuals with the same genetic mutation to be able to conduct a controlled experiment to understand the effect of RAD51 mutation on brain functions of individuals with congenital mirror movements. Second, with such a small sample size statistically significant differences may arise due to individual variability in brain anatomy (34). We therefore recruited 10 healthy controls to obtain normal distribution and increase our statistical power. Third, our study subjects do not have strictly balanced age and sex distribution, and hand preference is not equally represented. To be able to minimize the effect of age, sex, and hand preference on motor circuitry, demographic variables were kept constant between the patient group and healthy control group as in the literature (2).
In conclusion, we have found widespread functional abnormalities in brain structures of the motor loop in CMMD patients with RAD51 mutation. Our findings suggest that mirror movements are highly correlated with abnormal neuronal activity not only in cortex but also in subcortical structures during the performance of unimanual finger movements. These findings highlight the critical roles of different components and connections in the motor system to accomplish coordinated unimanual movements in healthy individuals.
This work was funded by a grant of the Turkish National Scientific and Technological Council (TUBI-TAK 1001- 108S355).
Conflict of interest disclosure
The authors declared no conflicts of interest.
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Onur Emre Onat
Aslihan Ors Gevrekci
From the Neuroscience Graduate Program (P.D. firstname.lastname@example.org, K.D., H.B.),A.S. Brain Research Center and National Magnetic Resonance Research Center (P.D., K.D., H.B.), and the Departments of Molecular Biology and Genetics (O.E.O., T.O.) and Psychology (K.D., H.B.), Bilkent University, Ankara, Turkey; Department of Psychology (A.O.G.), Baskent University, Ankara, Turkey; Department of Genome Sciences (S.G.), University of Washington, Seattle, WA, USA; Department of Neurology (H.U.), Akdeniz University School of Medicine, Antalya, Turkey; Department of Neurology (R.B.), Bezmialem University School of Medicine, Istanbul, Turkey; Department of Psychology (K.D., H.B.), JL Giessen University, Giessen, Germany.
Received 8 March 2018; revision requested 28 March 2018; last revision received 30 April 2018; accepted 6 May 2018.
You may cite this article as: Demirayak P, Onat OE, Ors Gevrekci A, et al. Abnormal subcortical activity in congenital mirror movement disorder with RAD51 mutation. Diagn Interv Radiol 2018; 24:392-401.
* Congenital mirror movement disorders (CMMD) are closely related to abnormal primary motor cortex and supplementary motor area activity during unimanual movements.
* Increased bilateral activity is present in CMMD patients in thalamus, striatum, and globus pallidus during unimanual movements.
* Activity of subcortical nuclei was higher in CMMD patients, which shows that involvement of these structures is also critical for unimanual movements.
Table 1. MNI coordinates of the center of the spherical ROIs that were used in task-based fMRI comparisons Region MNI coordinates (x, y, z) Left primary motor cortex -42, -16, 52 Right primary motor cortex 39, -22, 52 Left supplementary motor area -9, -16, 67 Right supplementary motor area 12, -16, 67 Left thalamus -12, -19, 4 Right thalamus 12, -19, 4 Left putamen -21, 8, -5 Right putamen 24, 8, -5 Left caudate -15, 14, 10 Right caudate 15, 14, 10 Left globus pallidus -15, -4, -5 Right globus pallidus 18, -4, -5 MNI, Montreal Neurological Institute; fMRI, functional magnetic resonance imaging. Table 2. Demographic characteristics and summary of the unimanual task-based fMRI comparisons ANOVA F(1,10) Factor 1: Factor 2: Factor 3: CMMD Controls Group Task Hemisphere n 2 10 - - - Sex (M/F) 2/0 10/0 - - - Age (y) 29.5 30.9[+ or -]5.04 - - - M1 - - 10.761 (b) 0.018 0.019 SMA - - 0.822 0.077 6.884 (a) THA - - 8.686 (a) 0.049 0.064 GP - - 4.893 0.487 0.586 STR - - 7.069 (a) 0.769 0.868 t statistics Interaction t (df=10) n - - Sex (M/F) - - Age (y) - 0.377 (10) M1 factor 2 X factor 3 L M1:-2.686 (a) 20.235 (b) R M1:-4.014 (b) SMA factor 2 X factor 3 NS 5.666 (a) factor 1 X factor 3 9.225 (a) THA factor 2 X factor 3 L THA:-2.935 (a) 10.028 (a) R THA:-2.495 (a) GP NS NS STR NS R STR:-3.337 (b) fMRI, functional magnetic resonance imaging; ANOVA, analysis of variance; CMMD, congenital mirror movement disorder; M, male; F, female; NS, not signifcant; M1, primary motor cortex; L, left, R, right; SMA, supplementary motor area; THA, thalamus; G P, globus pallidus; STR, striatum. (a) P < 0.05, (b) P < 0.01, (c) P < 0.001.
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|Title Annotation:||ORIGINAL ARTICLE|
|Author:||Demirayak, Pinar; Onat, Onur Emre; Gevrekci, Aslihan Ors; Gulsuner, Suleyman; Uysal, Hilmi; Bilgen,|
|Publication:||Diagnostic and Interventional Radiology|
|Date:||Nov 1, 2018|
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