Finger Tapping-Related Activation Differences in Treatment-Naive Pediatric Tourette Syndrome: A Comparison of the Preferred and Nonpreferred Hand
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| Title: | Finger Tapping-Related Activation Differences in Treatment-Naive Pediatric Tourette Syndrome: A Comparison of the Preferred and Nonpreferred Hand |
|---|---|
| Language: | English |
| Authors: | Roessner, Veit, Wittfoth, Matthias, August, Julia M., Rothenberger, Aribert, Baudewig, Jurgen, Dechent, Peter |
| Source: | Journal of Child Psychology and Psychiatry. Mar 2013 54(3):273-279. |
| Availability: | Wiley-Blackwell. 350 Main Street, Malden, MA 02148. Tel: 800-835-6770; Tel: 781-388-8598; Fax: 781-388-8232; e-mail: cs-journals@wiley.com; Web site: http://www.wiley.com/WileyCDA/ |
| Peer Reviewed: | Y |
| Page Count: | 7 |
| Publication Date: | 2013 |
| Document Type: | Journal Articles Reports - Research |
| Descriptors: | Neurological Impairments, Foreign Countries, Males, Early Adolescents, Preadolescents, Brain Hemisphere Functions, Diagnostic Tests, Human Body, Motion, Attention Deficit Hyperactivity Disorder, Symptoms (Individual Disorders), Handedness, Severity (of Disability), Comparative Analysis, Correlation, Behavior Disorders, Hypothesis Testing, Observation, Semi Structured Interviews |
| Geographic Terms: | Germany |
| Assessment and Survey Identifiers: | Edinburgh Handedness Inventory, Strengths and Difficulties Questionnaire, Wechsler Intelligence Scale for Children |
| DOI: | 10.1111/j.1469-7610.2012.02584.x |
| ISSN: | 0021-9630 |
| Abstract: | Background: Disturbances of motor circuitry are commonly encountered in Tourette syndrome (TS). The aim of this study was to investigate simple motor performance differences between boys with TS and healthy controls. Methods: We attempted to provide insight into motor network alterations by studying a group of treatment-naive patients suffering from "pure" TS, i.e., without comorbid symptomatology at an early stage of disease. We used functional MRI to compare activation patterns during right (preferred) and left (nonpreferred) index finger tapping between 22 TS boys (12.6 plus/minus 1.7 years) and 22 age-matched healthy control boys. Results: Boys with TS revealed altered motor network recruitment for right (dominant) and left (nondominant) index finger tapping. Brain activation patterns in response to index finger tapping of the nonpreferred left hand reflected the most prominent differences, including activation decrease in contralateral sensorimotor cortex while recruiting premotor and prefrontal regions along with the left inferior parietal lobule to a greater extent. Conclusions: This study demonstrates clear functional differences of simple index finger tapping in early-stage TS. We suggest that this reflects the requirement for additional brain networks to keep a normal performance level during the actual task and adaptive mechanisms due to continuous tic suppression and performance in TS. (Contains 2 tables and 1 figure.) |
| Abstractor: | As Provided |
| Number of References: | 38 |
| Entry Date: | 2014 |
| Accession Number: | EJ1012810 |
| Database: | ERIC |
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| FullText | Links: – Type: pdflink Url: https://content.ebscohost.com/cds/retrieve?content=AQICAHj0k_4E0hTGH8RJwT4gCJyBsGNe_WN95AvKlDbXJGqwxwFtsng4-cMV_EHAwrRPPnCJAAAA4jCB3wYJKoZIhvcNAQcGoIHRMIHOAgEAMIHIBgkqhkiG9w0BBwEwHgYJYIZIAWUDBAEuMBEEDChC1VsrM4MsTqpTYQIBEICBmgdKBZg-yuLRT4wWY6sPECkRsu1dAH5AMLYe_gJ7xyYv-uJo4jtDtLhHNW89OFqoXYzn49JClXZzAPveUBvqP1oLZujJ_Qqt9KNDiOzxRiG_lGDDM7C0BC-4_UMS9ii2-CeBNTq8WsRCSZBUORkwoLZjIeS6llBeV_Drt4HUKKApneUegQMs2M8towERy2cPTbPwP1GdAqxOW4M= Text: Availability: 1 Value: <anid>AN0085400384;jyy01mar.13;2024Jun04.07:33;v2.2.500</anid> <title id="AN0085400384-1">Finger tapping-related activation differences in treatment-naïve pediatric Tourette syndrome: a comparison of the preferred and nonpreferred hand. </title> <p>Background: Disturbances of motor circuitry are commonly encountered in Tourette syndrome (TS). The aim of this study was to investigate simple motor performance differences between boys with TS and healthy controls. Methods: We attempted to provide insight into motor network alterations by studying a group of treatment‐naïve patients suffering from ‘pure’ TS, i.e., without comorbid symptomatology at an early stage of disease. We used functional MRI to compare activation patterns during right (preferred) and left (nonpreferred) index finger tapping between 22 TS boys (12.6 ± 1.7 years) and 22 age‐matched healthy control boys. Results: Boys with TS revealed altered motor network recruitment for right (dominant) and left (nondominant) index finger tapping. Brain activation patterns in response to index finger tapping of the nonpreferred left hand reflected the most prominent differences, including activation decrease in contralateral sensorimotor cortex while recruiting premotor and prefrontal regions along with the left inferior parietal lobule to a greater extent. Conclusions: This study demonstrates clear functional differences of simple index finger tapping in early‐stage TS. We suggest that this reflects the requirement for additional brain networks to keep a normal performance level during the actual task and adaptive mechanisms due to continuous tic suppression and performance in TS.</p> <p>motor network; tourette syndrome; primary sensorimotor cortex; children; Finger tapping</p> <p>Tourette syndrome (TS) is characterized by multiple motor and vocal tics fluctuating in frequency, location, and severity while having its typical onset during childhood (Leckman, Bloch, Scahill, &amp; King, 2006). Increasing evidence of structural and functional investigations suggests that TS is associated with an underlying dynamic dysfunction of cortico‐striatal‐thalamic‐cortico (CSTC) neural circuitry (Makki, Govindan, Wilson, Behen, &amp; Chugani, 2009; Saporta et al., 2009). However, the exact nature of this dysfunction, and whether it has its roots in the basal ganglia, the cortex, or an imbalance between these two, is presently unresolved possibly to several confounders that are common in subjects with TS: First, coexisting psychiatric conditions especially attention‐deficit/hyperactivity disorder (ADHD) and obsessive‐compulsive disorders (OCD) are rather the rule than the exception in TS (Freeman et al., 2000) and have confounded some findings (Rothenberger, Roessner, Banaschewski, &amp; Leckman, 2007). Second, the common inclusion of adult subjects might be problematic, because long‐term consequences of extensive symptomatic medication exposure as well as of daily tic suppression and performance cannot be differentiated from etiologic factors more specific to TS per se. Moreover, the group of adults still suffering from TS represents only a specific minority of TS patients in view of the high rate of tic remission during late adolescence and early adulthood (Bloch et al., 2006).</p> <p>To avoid the unclear impact of the commonly coexisting conditions as well as previous and actual medication, we included a sample of treatment‐naïve boys suffering from ‘pure’ TS, i.e., without any comorbidity. Moreover, we recruited boys of an age as close as possible to the onset of first tics to minimize long‐term consequences of continuous tic performance and suppression without compliance problems. However, it has to be noted that the majority of them have suffered approximately half of their life from tics. Herein, we used a simple finger tapping task to study the neural correlates of simple motor performance in boys suffering from TS.</p> <p>Finger tapping tasks are an intensely used instrument to examine the human motor system. In addition, they have the advantage of being simple enough to be used in children as well as in patients with pathology of the motor system (Mostofsky et al., 2006). A recent meta‐analysis of finger tapping task variations identified regions of a brain network consisting of clusters in the primary sensorimotor cortex (SM1), supplementary motor area (SMA), premotor cortex, inferior parietal cortices, basal ganglia, and cerebellum (Witt, Laird, &amp; Meyerand, 2008). Findings of motor performance in TS have been inconsistent (e.g., (Biswal et al., 1998; Fattapposta et al., 2005), which might possibly be determined by methodological differences and the small number of subjects included (Schultz et al., 1998). Nevertheless, the preponderance of evidence supports the view of a dysfunction of the neural CSTC circuits (Bloch et al., 2006; Singer &amp; Minzer, 2003). Based on transcranial magnetic stimulation (TMS) findings, a recent study (Heise et al., 2010) proposed a model of deficient inhibition of the motor cortex at rest leading to higher occurrence of tics while stronger inhibition is thought to reflect compensatory functional mechanisms to regain control over motorcortical excitability during motor performance. On the basis of this view, we hypothesize that boys suffering from TS differ with regard to the recruitment of motor network brain regions compared with healthy control boys. More specifically, we hypothesize that the SM1 as an important region of motor execution will be less activated in patients; whereas other regions of the CSTC will be activated to a greater extend to compensate disorder‐related motor network dysfunction.</p> <hd id="AN0085400384-2">Methods</hd> <p>We recruited 22 treatment‐naïve boys (mean age 12.6 ± 1.7 years; range 10.2–14.2 years) with ‘pure’ TS, according to DSM‐IV and the Yale Global Tic Severity Scale (YGTSS) (Leckman et al., 1989), consecutively from the outpatient clinic of the Department of Child and Adolescent Psychiatry of the University of Goettingen as well as via the homepage of the German Tourette Syndrome Association. The outpatient clinic of the Department of Child and Adolescent Psychiatry of the University of Goettingen is a well‐known tertiary care center for TS in Germany since many years. Twenty‐two age‐ and IQ‐matched (measured using the Wechsler Intelligence Scale for Children‐Revised (WISC‐R)) healthy boys (mean age 12.8 ± 1.7 years; range 10.3–14.1 years) were recruited as controls from a youth club and school classes in Goettingen (for a detailed description of both groups see supplementary Table S1).</p> <p>Best‐estimate diagnoses were established on the basis of clinical observation, a German semi‐structured interview with parents and children (BADO) and various clinical ratings (parents, teachers, experts). The BADO (Noterdaeme et al., 2003) is based on a multiaxial classification system that is a long‐established national standard in child and adolescent psychiatry in Germany. Broadband psychopathology was screened by parent‐ and self‐rated Strength and Difficulties Questionnaires (SDQ; Goodman, 1997)). Parent ratings of symptoms of ADHD according to DSM‐IV were assessed with the ADHD Symptom Checklist (FBB‐HKS). This German 20‐item checklist has two subscales (inattention and hyperactivity/ impulsivity) and one total score, and was slightly superior to the Conners ADHD Index (Erhart, Dopfner, &amp; Ravens‐Sieberer, 2008). Obsessive‐compulsive symptoms were assessed by the Leyton Obsessional Inventory – Child Version (LOI‐CV; Berg, Whitaker, Davies, Flament, &amp; Rapoport, 1988). All diagnoses were verified in a case conference by senior board‐certified child psychiatrists (AR and VR) who have been working in clinical and research settings for TS and ADHD/OCD for many years.</p> <p>All subjects were right‐handers as indicated by the Edinburgh Handedness Inventory (Oldfield, 1971) and had normal or corrected to normal vision. Informed consent was obtained from all participating subjects and their parents. The study protocol was approved by the local Ethics Committee.</p> <p>During functional MRI, each participant performed alternating blocks of simple right‐hand and left‐hand index finger tapping onto a rigid board at a frequency of about 2 Hz. The order of the blocks was counterbalanced across participants. Finger tapping and rest periods were indicated by a green or a red dot, which participants viewed via a set of MR compatible LCD goggles (Resonance Technology, Northridge, CA, USA). A short practice session was applied before scanning to assure that participants understood the instruction and were able to correctly perform the finger tapping. Following an initial rest block, the experiment consisted of eight motor performance blocks (12 s) and eight resting periods (18 s) in alternating order. Thus, the total scanning time was 4 min and 18 s. Movement execution was monitored by the experimenter. No mirror movements could be observed.</p> <p>MRI was carried out at 3 Tesla (Magnetom Trio, Siemens Healthcare, Erlangen, Germany) using the standard 8 channel phased array head coil. T1‐weighted high‐resolution anatomical images were acquired for each participant (3D Turbo FLASH, repetition time (TR) 1,950 ms, inversion time 1,100 ms, echo time (TE) 3.92 ms, flip angle 12°). For the functional images, 129 volumes were acquired using single‐shot echo‐planar imaging (EPI), with an in‐plane resolution of 2 × 2 mm<sups>2</sups> (TR 2,000 ms, TE 36 ms, flip angle 70°, matrix 96 × 128). Each volume was oriented parallel to the AC‐PC plane and composed of 22 continuous 4‐mm thick slices covering the whole brain.</p> <p>Functional MRI data processing was carried out using BrainVoyager QX (Brain Innovation, Maastricht, The Netherlands). The data were corrected for slice scan time and three‐dimensional head movement; linear trends were removed and a high‐pass filter with 3 cycles/ unit in time course was applied. Spatial smoothing was achieved by applying a Gaussian filter with full width at half maximum (FWHM) = 5.0 mm. A general linear model approach was used for voxel‐wise first‐level single subject analysis, which involved the deconvolution of the block design with a two‐gamma function to model the hemodynamic response (Friston et al., 1998). Second level statistics were conducted using a random effects model with the first‐level single subject results for each group (TS and healthy controls) for left and right motor performance, respectively. Main effects for each movement condition were calculated in an analysis‐of‐variance (ANOVA). We calculated contrasts for right index finger tapping versus rest, left index finger tapping versus rest, as well as between‐group comparisons (TS patients vs. controls for each side, respectively). To correct for multiple comparisons, the cluster‐level statistical threshold estimation procedure was applied (Forman et al., 1995). In a first step, the activation maps were thresholded at p &lt; 0.001 for main effects (finger tapping vs. rest) and p &lt; 0.005 for between‐group effects. In a second step, the corresponding minimum activation cluster sizes yielding a p &lt; 0.05 (corrected for multiple comparisons) were calculated for each activation map separately, resulting in minimum cluster sizes of 81 mm<sups>3</sups> to 162 mm<sups>3</sups>. Assignment to anatomical brain regions was achieved using the Talairach Deamon (<ulink href="http://www.talairach.org/client.html">http://www.talairach.org/client.html</ulink>), the local maximum coordinates being taken as the crucial point.</p> <hd id="AN0085400384-3">Results</hd> <p>With regard to disorders commonly comorbid with TS, the specific instruments (ADHD: FBB‐HKS; OCD: LOI‐CV) did not reveal any group differences. All group means of the SDQ were within the lower normal range. This confirmed ‘pure’ TS in all affected boys.</p> <p>During right as well as left index finger tapping (compared with rest), boys with TS and healthy controls showed recruitment of motor‐related brain networks comprising the primary motor areas, premotor regions, and the basal ganglia.</p> <hd id="AN0085400384-4">Between‐group activations for right (preferred) and left (nonpreferred) index finger ...</hd> <p>The group comparison of right (preferred) index finger tapping revealed significant activation differences, specifically a higher signal increase for boys with TS in the left inferior parietal lobule (IPL). The reverse contrast showed more recruitment of the bilateral caudate nuclei and left middle frontal gyrus in controls (please see Figure 1and Table 1).</p> <p>1 Right index finger tapping: between‐group activations</p> <p> <ephtml> &lt;table&gt;&lt;tr&gt;&lt;th&gt;&amp;#x2003;&lt;/th&gt;&lt;th&gt;Hemisphere&lt;/th&gt;&lt;th&gt;Cluster size (mm&lt;sup&gt;3&lt;/sup&gt;)&lt;sup&gt;a&lt;/sup&gt;&lt;/th&gt;&lt;th&gt;t&amp;#x2010;Max&lt;/th&gt;&lt;th&gt;TalX&lt;/th&gt;&lt;th&gt;TalY&lt;/th&gt;&lt;th&gt;TalZ&lt;/th&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;Boys with Tourette syndrome greater than healthy controls&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Inferior parietal lobule&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;878&lt;/td&gt;&lt;td&gt;3.89&lt;/td&gt;&lt;td&gt;&amp;#x2212;45&lt;/td&gt;&lt;td&gt;&amp;#x2212;31&lt;/td&gt;&lt;td&gt;34&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;Healthy controls greater than boys with Tourette syndrome&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td valign="top"&gt;&amp;#x2003;Caudate&lt;/td&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;396&lt;/td&gt;&lt;td&gt;4.18&lt;/td&gt;&lt;td&gt;21&lt;/td&gt;&lt;td&gt;26&lt;/td&gt;&lt;td&gt;16&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;395&lt;/td&gt;&lt;td&gt;3.46&lt;/td&gt;&lt;td&gt;&amp;#x2212;18&lt;/td&gt;&lt;td&gt;26&lt;/td&gt;&lt;td&gt;16&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Middle frontal gyrus&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;943&lt;/td&gt;&lt;td&gt;3.58&lt;/td&gt;&lt;td&gt;&amp;#x2212;27&lt;/td&gt;&lt;td&gt;26&lt;/td&gt;&lt;td&gt;22&lt;/td&gt;&lt;/tr&gt;&lt;/table&gt; </ephtml> </p> <p>1 aVoxel size was upsampled in Brainvoyager to 1 mm3 isotropic voxels.</p> <p>For the contrast ‘TS boys greater than healthy control boys’ during index finger tapping of the left (nonpreferred) hand, we found a widespread network of motor preparation and control, including activity bilaterally in the dorsolateral prefrontal cortex (DLPFC) and premotor areas (pre‐SMA and bilateral precentral gyri), and – again – in the left IPL.</p> <p>The inverse contrast revealed that healthy boys showed a greater recruitment of the right SM1 during left index finger tapping compared with boys suffering from TS (please see Table 2).</p> <p>2 Left index finger tapping: between‐group activations</p> <p> <ephtml> &lt;table&gt;&lt;tr&gt;&lt;th&gt;&amp;#x2003;&lt;/th&gt;&lt;th&gt;Hemisphere&lt;/th&gt;&lt;th&gt;Cluster size (mm&lt;sup&gt;3&lt;/sup&gt;)&lt;sup&gt;a&lt;/sup&gt;&lt;/th&gt;&lt;th&gt;t&amp;#x2010;Max&lt;/th&gt;&lt;th&gt;TalX&lt;/th&gt;&lt;th&gt;TalY&lt;/th&gt;&lt;th&gt;TalZ&lt;/th&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;Boys with Tourette syndrome greater than healthy controls&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td valign="top"&gt;&amp;#x2003;Medial frontal gyrus&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;1,009&lt;/td&gt;&lt;td&gt;4.03&lt;/td&gt;&lt;td&gt;&amp;#x2212;3&lt;/td&gt;&lt;td&gt;&amp;#x2212;19&lt;/td&gt;&lt;td&gt;58&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;1,027&lt;/td&gt;&lt;td&gt;3.67&lt;/td&gt;&lt;td&gt;&amp;#x2212;15&lt;/td&gt;&lt;td&gt;26&lt;/td&gt;&lt;td&gt;40&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;815&lt;/td&gt;&lt;td&gt;3.37&lt;/td&gt;&lt;td&gt;6&lt;/td&gt;&lt;td&gt;50&lt;/td&gt;&lt;td&gt;37&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td valign="top"&gt;&amp;#x2003;Superior frontal gyrus&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;902&lt;/td&gt;&lt;td&gt;3.92&lt;/td&gt;&lt;td&gt;&amp;#x2212;18&lt;/td&gt;&lt;td&gt;41&lt;/td&gt;&lt;td&gt;28&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;903&lt;/td&gt;&lt;td&gt;3.63&lt;/td&gt;&lt;td&gt;9&lt;/td&gt;&lt;td&gt;53&lt;/td&gt;&lt;td&gt;28&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Pre&amp;#x2010;SMA&lt;/td&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;1,078&lt;/td&gt;&lt;td&gt;3.84&lt;/td&gt;&lt;td&gt;6&lt;/td&gt;&lt;td&gt;20&lt;/td&gt;&lt;td&gt;55&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td valign="top"&gt;&amp;#x2003;Precentral gyrus&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;682&lt;/td&gt;&lt;td&gt;5.02&lt;/td&gt;&lt;td&gt;&amp;#x2212;36&lt;/td&gt;&lt;td&gt;2&lt;/td&gt;&lt;td&gt;22&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;683&lt;/td&gt;&lt;td&gt;3.78&lt;/td&gt;&lt;td&gt;30&lt;/td&gt;&lt;td&gt;2&lt;/td&gt;&lt;td&gt;31&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td valign="top"&gt;&amp;#x2003;Dorsolateral prefrontal cortex&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;943&lt;/td&gt;&lt;td&gt;4.64&lt;/td&gt;&lt;td&gt;&amp;#x2212;30&lt;/td&gt;&lt;td&gt;29&lt;/td&gt;&lt;td&gt;25&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;697&lt;/td&gt;&lt;td&gt;3.88&lt;/td&gt;&lt;td&gt;&amp;#x2212;45&lt;/td&gt;&lt;td&gt;41&lt;/td&gt;&lt;td&gt;23&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;900&lt;/td&gt;&lt;td&gt;4.98&lt;/td&gt;&lt;td&gt;42&lt;/td&gt;&lt;td&gt;5&lt;/td&gt;&lt;td&gt;22&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Anterior cingulate cortex&lt;/td&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;942&lt;/td&gt;&lt;td&gt;3.93&lt;/td&gt;&lt;td&gt;12&lt;/td&gt;&lt;td&gt;&amp;#x2212;1&lt;/td&gt;&lt;td&gt;46&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Middle temporal gyrus&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;703&lt;/td&gt;&lt;td&gt;5.04&lt;/td&gt;&lt;td&gt;&amp;#x2212;42&lt;/td&gt;&lt;td&gt;&amp;#x2212;55&lt;/td&gt;&lt;td&gt;7&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Posterior cingulate&lt;/td&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;916&lt;/td&gt;&lt;td&gt;4.82&lt;/td&gt;&lt;td&gt;15&lt;/td&gt;&lt;td&gt;&amp;#x2212;19&lt;/td&gt;&lt;td&gt;40&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Insula&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;447&lt;/td&gt;&lt;td&gt;4.75&lt;/td&gt;&lt;td&gt;&amp;#x2212;48&lt;/td&gt;&lt;td&gt;&amp;#x2212;40&lt;/td&gt;&lt;td&gt;19&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Lingual gyrus&lt;/td&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;482&lt;/td&gt;&lt;td&gt;3.88&lt;/td&gt;&lt;td&gt;21&lt;/td&gt;&lt;td&gt;&amp;#x2212;40&lt;/td&gt;&lt;td&gt;&amp;#x2212;2&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Middle occipital gyrus&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;306&lt;/td&gt;&lt;td&gt;4.5&lt;/td&gt;&lt;td&gt;&amp;#x2212;27&lt;/td&gt;&lt;td&gt;&amp;#x2212;79&lt;/td&gt;&lt;td&gt;&amp;#x2212;2&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Inferior parietal lobule&lt;/td&gt;&lt;td&gt;L&lt;/td&gt;&lt;td&gt;878&lt;/td&gt;&lt;td&gt;3.38&lt;/td&gt;&lt;td&gt;&amp;#x2212;54&lt;/td&gt;&lt;td&gt;&amp;#x2212;28&lt;/td&gt;&lt;td&gt;25&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;Healthy controls greater than boys with Tourette syndrome&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td&gt;&amp;#x2003;Sensorymotor cortex&lt;/td&gt;&lt;td&gt;R&lt;/td&gt;&lt;td&gt;896&lt;/td&gt;&lt;td&gt;4.54&lt;/td&gt;&lt;td&gt;36&lt;/td&gt;&lt;td&gt;&amp;#x2212;31&lt;/td&gt;&lt;td&gt;61&lt;/td&gt;&lt;/tr&gt;&lt;/table&gt; </ephtml> </p> <ulist> <item>2 SMA, supplementary motor area.</item> <item>3 aVoxel size was upsampled in Brainvoyager to 1 mm3 isotropic voxels.</item> </ulist> <hd id="AN0085400384-5">Correlation of between‐group brain activity and tic severity (YGTSS)</hd> <p>To relate our findings of between‐group differences to tic severity, we built ROIs (regions of interest) of the resulting brain areas, and correlated the mean extracted signal value of each TS boy with his individual YGTSS score. We found significant correlations only for the left‐hand finger tapping, but not for the right‐hand finger tapping. Beside an activation cluster in the right medial frontal gyrus (r = 0.48, p = 0.02), we found that left superior frontal gyrus (r = 0.52, p = 0.01) and the right Pre‐SMA (r = 0.45, p = 0.03) significantly correlated with tic severity.</p> <hd id="AN0085400384-6">Discussion</hd> <p>The overall aim of this study was to explore the activation patterns during a simple index finger tapping task. The simplicity of the motor task that has been shown to be a useful and reliable instrument (Lee et al., 2010) enabled us to obtain robust information about the functional dynamics of key motor regions. The inclusion of young treatment‐naïve right‐handed boys suffering from ‘pure’ TS as close as possible to the onset of first tics without compliance problems minimized confounding effects due to comorbid symptomatology as well as long‐term consequences of tic performance and suppression. Therefore, comparing them with a healthy gender‐, age‐, handedness‐, and IQ‐matched control group enabled us to test the hypothesis of different recruitment of motor network areas specifically for ‘pure’ TS. In fact, as the right finger tapping motor performance of right‐handers is usually easier to accomplish (Horenstein, Lowe, Koenig, &amp; Phillips, 2009), a comparison of finger tapping execution between the right (preferred) and the more difficult left (nonpreferred) index finger should enable us to draw conclusion about the underlying altered motor network in TS, which might be influenced by task difficulty.</p> <p>The main findings of this study can be summarized as follows: The comparison between the two groups revealed significant activation differences during right (preferred) index finger tapping. In particular, our observations include a higher recruitment of the left IPL in TS, whereas the caudate, as well as the middle frontal gyrus were recruited to a lesser extent. The finding of decreased activity in the caudate is a little bit puzzling, as our group recently found an increase of activation in the caudate during the comparison of solely right index finger tapping in a comparable cohort of young boys suffering from TS (Roessner et al., 2012). This discrepancy might be solved by looking at the hemispheric preponderance of this activation. In this study, there was a bilateral caudate signal decrease in TS boys. In our previous study, we observed a left‐sided caudate recruitment. Although, structural and functional results highlighted the importance of the basal ganglia in the specific pathology of TS, their roles in motor performance and control are much debated still (Lee et al., 2010; Turner &amp; Desmurget, 2010). With regard to the higher activity of the left IPL in TS boys, our results indicate a common mechanism of keeping the motor performance at a normal level, as we found the IPL to be activated irrespective of finger tapping side. On the background of theories of IPL function, we speculate that these processes might deal with attention allocation and suggest a more effortful (less automatic) performance mode (Jancke, Loose, Lutz, Specht, &amp; Shah, 2000). Moreover, the IPL has been associated with high‐level visuomotor representations, and in particular, the left IPL is thought to store complex representations of actions (Fogassi &amp; Luppino, 2005).</p> <p>During left (nonpreferred) index finger tapping boys suffering from TS showed less activity in contralateral right SM1 compared with healthy controls, while recruiting several other regions to a greater extent. These regions are part of the brain network of motor preparation and control, including activity bilaterally in the DLPFC and premotor areas, and – as mentioned above – in the left IPL.</p> <p>Our results indicate that treatment‐naïve boys with ‘pure’ TS show altered motor network activations during simple motor performance. These alterations were more pronounced when finger movements were executed with the left hand. The view of a different recruitment of motor network areas in TS, and especially the finding that contralateral SM1 is activated to a lesser extent compared with healthy controls, is supported by a recently proposed model of altered motor cortex excitability in TS (Heise et al., 2010). This view suggests that in TS, there is a disinhibition of motorcortical regions at rest, which leads to an abnormally disinhibited level of short‐interval intracortical inhibition at the beginning of the movement preparation phase. During motor performance, complex motor areas and prefrontal cortex exercise control over this increased excitability by overriding anomalous subcortical inputs. Thus, as TS patients start from a higher motorcortical level than healthy controls (see also Orth &amp; Rothwell, 2009), less activity in contralateral SM1 is seen. It seems that this difference is in particular relevant during the more difficult nondominant finger tapping condition.</p> <p>The widespread activations of premotor and prefrontal areas during the more difficult left (nonpreferred) finger tapping indicate that for TS patients more effort might be necessary to keep up the appropriate performance level. According to the additional top‐down control of complex motor areas during motor performance, we also found that the pre‐SMA revealed greater signal increases in boys suffering from TS compared with healthy control children. In particular, the pre‐SMA has been shown to play an important role for the self‐initiation of movements (Rowe, Hughes, &amp; Nimmo‐Smith, 2010). Its higher recruitment in TS as well as the correlation with tic severity suggests an important role of this area, in particular when performing motor acts with the more difficult nondominant left side. Additional DLPFC activity might indicate a supportive role during successful motor performance.</p> <p>A recent study with adults suffering from TS (Werner et al., 2011) also reported functional activation differences compared with a matched control group with regard to the more difficult left‐hand finger tapping task. In particular, they found a widespread activation pattern of signal increases in the patient, which is comparable with our results, although not the same. Interestingly, they observed no functional alterations in SM1. This evidence might be one of the key differences between juvenile and adults TS patients.</p> <p>An alternative explanation might be derived from observations of structural abnormalities (Fahim et al., 2009; Sowell et al., 2008), indicating that patients suffering from TS have smaller motor areas. However, a recent study from our group failed to find significant structural differences using voxel‐based morphometry in a comparable TS‐group of treatment‐naïve boys (Roessner et al., 2009) indicating that close to the onset of the disorder, the relationship between short‐term functional and structural neuroplastic compensations still remain unclear and should be an important issue of future investigations (Plessen, Bansal, &amp; Peterson, 2009). Again, it is crucial to emphasize the role of confounding variables (e.g., comorbid symptomatology, medication status), which has to be thoroughly considered.</p> <p>The lack of behavioral performance measures during fMRI (however, in a prescanning practice session, no differences could be found) as well as the possible confound of tic suppression during finger tapping must be mentioned as limiting factors for the interpretation of our study. Unfortunately, a video‐system that allows monitoring the bodies of our participants while lying in the scanner without affecting image quality was not available in our lab. Such a system has been shown to be valuable, in particular for these kinds of patients groups (Neuner et al., 2007). At last, we want to stress that studying only boys with ‘pure’ TS on the one hand, strengthens the specificity of these findings for the etiopathophysiology of TS. On the other hand, it limits the degree to which these findings can be generalized to a typical sample of TS patients in daily clinical care.</p> <p>Together with recent studies, which suggest a TS‐associated immature development of functional connections of the fronto‐parietal and fronto‐striatal network (Church et al., 2009; Makki et al., 2009; Marsh, Zhu, Wang, Skudlarski, &amp; Peterson, 2007; Raz et al., 2009), our findings corroborate the view of short‐term compensatory mechanisms most likely in response to continuous tic suppression and performance, which are reflected in altered motor network activations. Taken together, our observations indicate that TS‐induced motor network changes consequentially let patients treat even simple motor tasks, as if they need more complex planning and organization of motor performance, in particular when executed with the nondominant hand.</p> <hd id="AN0085400384-7">Acknowledgements</hd> <p>We thank all participating persons and their families for their great support, as well as three anonymous reviewers for helpful comments. There was no financial support for this study; see title page footnote for disclosure of potential conflicts of interest.</p> <hd id="AN0085400384-8">Correspondence</hd> <p>Matthias Wittfoth, Department of Neurology, Hannover Medical School, Hannover, Germany; Email: wittfoth.matthias@mh-hannover.de</p> <hd id="AN0085400384-9">Key points</hd> <p>• Findings of motor performance in TS have been inconsistent.</p> <p>• Neural response patterns of finger tapping were compared between boys with Tourette syndrome (TS) and controls.</p> <p>• Brain activation patterns in response to the nonpreferred left hand index finger tapping reflected the most prominent differences.</p> <p>• Herein, less activity in contralateral SM1 was found.</p> <p>• Additional recruitment of left IPL in both conditions (right and left index finger tapping) might reflect increased effort of motor performance.</p> <p>Table S1 Group characteristics of the participating boys</p> <ref id="AN0085400384-10"> <title>Footnotes</title> <blist> <bibl id="bib1" type="bt">1</bibl> <bibtext>Both authors contributed equally to this work. </bibtext> </blist> <blist> <bibl id="bib2" type="bt">2</bibl> <bibtext>Present address: Department of Child and Adolescent Psychiatry, University Medical Center, Dresden, Germany </bibtext> </blist> <blist> <bibl id="bib3" type="bt">3</bibl> <bibtext>Present address: Dahlem Institute for Neuroimaging of Emotion, Cluster of Excellence “Languages of Emotion”, Freie Universitaet Berlin, Germany </bibtext> </blist> <blist> <bibl id="bib4" type="bt">4</bibl> <bibtext>Conflict of interest statement: Professor Rothenberger reports having received research and travel support, as well as an educational grant from Shire (German Research Society, Schwaabe). He is in the advisory board and speakers’ bureau of Lilly, Shire, Medice, and Novartis. He disclosed consulting fees from UCB/Shire, and Lilly. Professor Roessner reported honoraria for lectures from Lilly, Medice, Novartis, and Shire. He is in the advisory board of Lilly and Norvartis. Mrs. August, Dr. Wittfoth, Dr. Dechent, and Dr. Baudewig reported no financial relationships with commercial interests. </bibtext> </blist> </ref> <ref id="AN0085400384-11"> <title>References</title> <blist> <bibtext>Berg, C.Z., Whitaker, A., Davies, M., Flament, M.F., &amp; Rapoport, J.L. ( 1988 ). The survey form of the Leyton Obsessional Inventory‐Child Version: norms from an epidemiological study. Journal of the American Academy of Child and Adolescent Psychiatry, 27, 759 – 763. </bibtext> </blist> <blist> <bibtext>Biswal, B., Ulmer, J.L., Krippendorf, R.L., Harsch, H.H., Daniels, D.L., Hyde, J.S., … &amp; Haughton, V.M. ( 1998 ). 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Neuroimage, 42, 343 – 356. </bibtext> </blist> </ref> <p>Graph: 1 Between‐group comparisons: Comparison of brain activations between boys suffering from Tourette syndrome (n = 22) and healthy control boys (n = 22). Statistical threshold maps were overlaid onto the averaged T1‐weighted brain of all subjects</p> <p>Graph: image%5fn/jcpp2584%5ff1.gif</p> <p>Graph: Supporting info item</p> <aug> <p>By Veit Roessner; Matthias Wittfoth; Julia M. August; Aribert Rothenberger; Jürgen Baudewig and Peter Dechent</p> </aug> |
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| Items | – Name: Title Label: Title Group: Ti Data: Finger Tapping-Related Activation Differences in Treatment-Naive Pediatric Tourette Syndrome: A Comparison of the Preferred and Nonpreferred Hand – Name: Language Label: Language Group: Lang Data: English – Name: Author Label: Authors Group: Au Data: <searchLink fieldCode="AR" term="%22Roessner%2C+Veit%22">Roessner, Veit</searchLink><br /><searchLink fieldCode="AR" term="%22Wittfoth%2C+Matthias%22">Wittfoth, Matthias</searchLink><br /><searchLink fieldCode="AR" term="%22August%2C+Julia+M%2E%22">August, Julia M.</searchLink><br /><searchLink fieldCode="AR" term="%22Rothenberger%2C+Aribert%22">Rothenberger, Aribert</searchLink><br /><searchLink fieldCode="AR" term="%22Baudewig%2C+Jurgen%22">Baudewig, Jurgen</searchLink><br /><searchLink fieldCode="AR" term="%22Dechent%2C+Peter%22">Dechent, Peter</searchLink> – Name: TitleSource Label: Source Group: Src Data: <searchLink fieldCode="SO" term="%22Journal+of+Child+Psychology+and+Psychiatry%22"><i>Journal of Child Psychology and Psychiatry</i></searchLink>. Mar 2013 54(3):273-279. – Name: Avail Label: Availability Group: Avail Data: Wiley-Blackwell. 350 Main Street, Malden, MA 02148. Tel: 800-835-6770; Tel: 781-388-8598; Fax: 781-388-8232; e-mail: cs-journals@wiley.com; Web site: http://www.wiley.com/WileyCDA/ – Name: PeerReviewed Label: Peer Reviewed Group: SrcInfo Data: Y – Name: Pages Label: Page Count Group: Src Data: 7 – Name: DatePubCY Label: Publication Date Group: Date Data: 2013 – Name: TypeDocument Label: Document Type Group: TypDoc Data: Journal Articles<br />Reports - Research – Name: Subject Label: Descriptors Group: Su Data: <searchLink fieldCode="DE" term="%22Neurological+Impairments%22">Neurological Impairments</searchLink><br /><searchLink fieldCode="DE" term="%22Foreign+Countries%22">Foreign Countries</searchLink><br /><searchLink fieldCode="DE" term="%22Males%22">Males</searchLink><br /><searchLink fieldCode="DE" term="%22Early+Adolescents%22">Early Adolescents</searchLink><br /><searchLink fieldCode="DE" term="%22Preadolescents%22">Preadolescents</searchLink><br /><searchLink fieldCode="DE" term="%22Brain+Hemisphere+Functions%22">Brain Hemisphere Functions</searchLink><br /><searchLink fieldCode="DE" term="%22Diagnostic+Tests%22">Diagnostic Tests</searchLink><br /><searchLink fieldCode="DE" term="%22Human+Body%22">Human Body</searchLink><br /><searchLink fieldCode="DE" term="%22Motion%22">Motion</searchLink><br /><searchLink fieldCode="DE" term="%22Attention+Deficit+Hyperactivity+Disorder%22">Attention Deficit Hyperactivity Disorder</searchLink><br /><searchLink fieldCode="DE" term="%22Symptoms+%28Individual+Disorders%29%22">Symptoms (Individual Disorders)</searchLink><br /><searchLink fieldCode="DE" term="%22Handedness%22">Handedness</searchLink><br /><searchLink fieldCode="DE" term="%22Severity+%28of+Disability%29%22">Severity (of Disability)</searchLink><br /><searchLink fieldCode="DE" term="%22Comparative+Analysis%22">Comparative Analysis</searchLink><br /><searchLink fieldCode="DE" term="%22Correlation%22">Correlation</searchLink><br /><searchLink fieldCode="DE" term="%22Behavior+Disorders%22">Behavior Disorders</searchLink><br /><searchLink fieldCode="DE" term="%22Hypothesis+Testing%22">Hypothesis Testing</searchLink><br /><searchLink fieldCode="DE" term="%22Observation%22">Observation</searchLink><br /><searchLink fieldCode="DE" term="%22Semi+Structured+Interviews%22">Semi Structured Interviews</searchLink> – Name: Subject Label: Geographic Terms Group: Su Data: <searchLink fieldCode="DE" term="%22Germany%22">Germany</searchLink> – Name: SubjectThesaurus Label: Assessment and Survey Identifiers Group: Su Data: <searchLink fieldCode="SU" term="%22Edinburgh+Handedness+Inventory%22">Edinburgh Handedness Inventory</searchLink><br /><searchLink fieldCode="SU" term="%22Strengths+and+Difficulties+Questionnaire%22">Strengths and Difficulties Questionnaire</searchLink><br /><searchLink fieldCode="SU" term="%22Wechsler+Intelligence+Scale+for+Children%22">Wechsler Intelligence Scale for Children</searchLink> – Name: DOI Label: DOI Group: ID Data: 10.1111/j.1469-7610.2012.02584.x – Name: ISSN Label: ISSN Group: ISSN Data: 0021-9630 – Name: Abstract Label: Abstract Group: Ab Data: Background: Disturbances of motor circuitry are commonly encountered in Tourette syndrome (TS). The aim of this study was to investigate simple motor performance differences between boys with TS and healthy controls. Methods: We attempted to provide insight into motor network alterations by studying a group of treatment-naive patients suffering from "pure" TS, i.e., without comorbid symptomatology at an early stage of disease. We used functional MRI to compare activation patterns during right (preferred) and left (nonpreferred) index finger tapping between 22 TS boys (12.6 plus/minus 1.7 years) and 22 age-matched healthy control boys. Results: Boys with TS revealed altered motor network recruitment for right (dominant) and left (nondominant) index finger tapping. Brain activation patterns in response to index finger tapping of the nonpreferred left hand reflected the most prominent differences, including activation decrease in contralateral sensorimotor cortex while recruiting premotor and prefrontal regions along with the left inferior parietal lobule to a greater extent. Conclusions: This study demonstrates clear functional differences of simple index finger tapping in early-stage TS. We suggest that this reflects the requirement for additional brain networks to keep a normal performance level during the actual task and adaptive mechanisms due to continuous tic suppression and performance in TS. (Contains 2 tables and 1 figure.) – Name: AbstractInfo Label: Abstractor Group: Ab Data: As Provided – Name: Ref Label: Number of References Group: RefInfo Data: 38 – Name: DateEntry Label: Entry Date Group: Date Data: 2014 – Name: AN Label: Accession Number Group: ID Data: EJ1012810 |
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| RecordInfo | BibRecord: BibEntity: Identifiers: – Type: doi Value: 10.1111/j.1469-7610.2012.02584.x Languages: – Text: English PhysicalDescription: Pagination: PageCount: 7 StartPage: 273 Subjects: – SubjectFull: Neurological Impairments Type: general – SubjectFull: Foreign Countries Type: general – SubjectFull: Males Type: general – SubjectFull: Early Adolescents Type: general – SubjectFull: Preadolescents Type: general – SubjectFull: Brain Hemisphere Functions Type: general – SubjectFull: Diagnostic Tests Type: general – SubjectFull: Human Body Type: general – SubjectFull: Motion Type: general – SubjectFull: Attention Deficit Hyperactivity Disorder Type: general – SubjectFull: Symptoms (Individual Disorders) Type: general – SubjectFull: Handedness Type: general – SubjectFull: Severity (of Disability) Type: general – SubjectFull: Comparative Analysis Type: general – SubjectFull: Correlation Type: general – SubjectFull: Behavior Disorders Type: general – SubjectFull: Hypothesis Testing Type: general – SubjectFull: Observation Type: general – SubjectFull: Semi Structured Interviews Type: general – SubjectFull: Germany Type: general – SubjectFull: Edinburgh Handedness Inventory Type: general – SubjectFull: Strengths and Difficulties Questionnaire Type: general – SubjectFull: Wechsler Intelligence Scale for Children Type: general Titles: – TitleFull: Finger Tapping-Related Activation Differences in Treatment-Naive Pediatric Tourette Syndrome: A Comparison of the Preferred and Nonpreferred Hand Type: main BibRelationships: HasContributorRelationships: – PersonEntity: Name: NameFull: Roessner, Veit – PersonEntity: Name: NameFull: Wittfoth, Matthias – PersonEntity: Name: NameFull: August, Julia M. – PersonEntity: Name: NameFull: Rothenberger, Aribert – PersonEntity: Name: NameFull: Baudewig, Jurgen – PersonEntity: Name: NameFull: Dechent, Peter IsPartOfRelationships: – BibEntity: Dates: – D: 01 M: 03 Type: published Y: 2013 Identifiers: – Type: issn-print Value: 0021-9630 Numbering: – Type: volume Value: 54 – Type: issue Value: 3 Titles: – TitleFull: Journal of Child Psychology and Psychiatry Type: main |
| ResultId | 1 |