Letters to the Editor [10] Cerasa A, Morelli M, Augimeri A, Salsone M, Novellino F, Gioia MC, et al. Prefrontal thickening in PD with levodopa-induced dyskinesias: new evidence from cortical thickness measurement. Parkinsonism Relat Disord 2013;19:123–5. [11] Vernon AC, Modo M. Do levodopa treatments modify the morphology of the parkinsonian brain? Mov Disord 2012;27:166–7. [12] Li CT, Chou KH, Su TP, Huang CC, Chen MH, Bai YM, et al. Gray matter abnormalities in schizophrenia patients with tardive dyskinesia: a magnetic resonance imaging voxel-based morphometry study. PLoS One 2013;8:e71034. http://dx.doi.org/ 10.1371/journal.pone.0071034. [13] Cerasa A, Quattrone A. May hyperdirect pathway be a plausible neural substrate for understanding the rTMS-related effects on PD patients with levodopa-induced dyskinesias? Brain Stimul 2014. http://dx.doi.org/10.1016/j.brs.2014.01.007.
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of voluntary action might be related to the presence of involuntary hyperkinesias is risky. Although distinct areas involved in voluntary action generation and action inhibition might be implicated in the pathogenesis of tics [18,19], channelling results from different studies exploring hyperkinesias of different aetiologies to common pathophysiological pathways carries the danger of oversimplification. Combining hypothesis-driven multimodal approaches in different clinical populations studied longitudinally will promote understanding of the delicate balance between involuntary movements and voluntary motor control. References
Antonio Cerasa UOS-IBFM, National Research Council, Catanzaro, Italy Corresponding author at: Consiglio Nazionale delle Ricerche (CNR), Unità di Ricerca Neuroimmagini, Catanzaro, 88100, Italy. Tel.: +39 0961 369 5904. E-mail addresses: [email protected]. Aldo Quattrone UOS-IBFM, National Research Council, Catanzaro, Italy Institute of Neurology, University “Magna Graecia”, Germaneto, CZ, Italy 18 February 2014
DOI of original article: http://dx.doi.org/10.1016/j.jpsychores.2013.10.014 http://dx.doi.org/10.1016/j.jpsychores.2014.03.009 0022 – 3999/$ – see front matter © 2014 Elsevier Inc. All rights reserved.
Reply to: The role of the inferior frontal cortex in hyperkinetic movement disorders
Sir, Gilles de la Tourette syndrome (GTS) is a neurodevelopmental disorder. Tics resemble normal motor behaviour, appearing uncontrollable and out of context. Tic production has been linked to either excess generation of movement, insufficient motor inhibition, or both [1]. Neuropathological studies of inhibitory interneuronal populations predominantly from sensorimotor parts of the striatum [2,3], as well as recordings of neuronal activity from animal models of tics and GTS patients have provided converging evidence that tics might indeed be excessively generated due to local disinhibition at subcortical levels [4–7]. However, the translation of these results to a general inhibitory deficit of motor behaviour, for example in inhibition of voluntary actions can be precarious. Several studies have demonstrated that GTS patients of different ages have normal action inhibition (i.e. commission errors) in Stop Signal Reaction Time (SSRT) and Go/NoGo tasks [8–10]. Also, some studies have suggested that GTS patients might in fact have enhanced control over their motor output, as an adaptation to having to suppress tics in different social situations over the years [11–13]. We showed that the ability to inhibit tics on demand does not correlate with grey matter volumes of the right inferior frontal cortex and left frontal pole. Nevertheless, grey matter volume in these areas was reduced compared to healthy controls [14]. This further confirms previous findings in adult GTS patients demonstrating decreased cortical volumes [15–17]. We suggest that grey matter volume reductions might represent trait characteristics of tic persistence into adulthood. In contrast, inhibition of tics on demand should be considered a state characteristic of behavioural motor performance. The assumption that brain structure corresponds in a one to one fashion to function and behavioural performance may be unwarranted. Also, the speculation that behavioural deficits in the inhibition
[1] Ganos C, Roessner V, Munchau A. The functional anatomy of Gilles de la Tourette syndrome. Neurosci Biobehav Rev 2013;37:1050–62. [2] Kalanithi PS, Zheng W, Kataoka Y, DiFiglia M, Grantz H, Saper CB, et al. Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc Natl Acad Sci U S A 2005;102:13307–12. [3] Kataoka Y, Kalanithi PS, Grantz H, Schwartz ML, Saper C, Leckman JF, et al. Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome. J Comp Neurol 2010;518:277–91. [4] Bronfeld M, Bar-Gad I. Tic disorders: what happens in the basal ganglia? Neuroscientist 2013;19:101–8. [5] Bronfeld M, Belelovsky K, Bar-Gad I. Spatial and temporal properties of tic-related neuronal activity in the cortico-basal ganglia loop. J Neurosci 2011;31:8713–21. [6] McCairn KW, Bronfeld M, Belelovsky K, Bar-Gad I. The neurophysiological correlates of motor tics following focal striatal disinhibition. Brain 2009;132:2125–38. [7] Zhuang P, Hallett M, Zhang X, Li J, Zhang Y, Li Y. Neuronal activity in the globus pallidus internus in patients with tics. J Neurol Neurosurg Psychiatry 2009;80:1075–81. [8] Roessner V, Albrecht B, Dechent P, Baudewig J, Rothenberger A. Normal response inhibition in boys with Tourette syndrome. Behav Brain Funct 2008;4:29. [9] Serrien DJ, Orth M, Evans AH, Lees AJ, Brown P. Motor inhibition in patients with Gilles de la Tourette syndrome: functional activation patterns as revealed by EEG coherence. Brain 2005;128:116–25. [10] Watkins LH, Sahakian BJ, Robertson MM, Veale DM, Rogers RD, Pickard KM, et al. Executive function in Tourette's syndrome and obsessive–compulsive disorder. Psychol Med 2005;35:571–82. [11] Jackson GM, Mueller SC, Hambleton K, Hollis CP. Enhanced cognitive control in Tourette syndrome during task uncertainty. Exp Brain Res 2007;182:357–64. [12] Jackson SR, Parkinson A, Jung J, Ryan SE, Morgan PS, Hollis C, et al. Compensatory neural reorganization in Tourette syndrome. Curr Biol 2011;21:580–5. [13] Mueller SC, Jackson GM, Dhalla R, Datsopoulos S, Hollis CP. Enhanced cognitive control in young people with Tourette's syndrome. Curr Biol 2006;16:570–3. [14] Ganos C, Kuhn S, Kahl U, Schunke O, Brandt V, Baumer T, et al. Prefrontal cortex volume reductions and tic inhibition are unrelated in uncomplicated GTS adults. J Psychosom Res 2014;76:84–7. [15] Draganski B, Martino D, Cavanna AE, Hutton C, Orth M, Robertson MM, et al. Multispectral brain morphometry in Tourette syndrome persisting into adulthood. Brain 2010;133:3661–75. [16] Muller-Vahl KR, Kaufmann J, Grosskreutz J, Dengler R, Emrich HM, Peschel T. Prefrontal and anterior cingulate cortex abnormalities in Tourette syndrome: evidence from voxel-based morphometry and magnetization transfer imaging. BMC Neurosci 2009;10:47. [17] Wittfoth M, Bornmann S, Peschel T, Grosskreutz J, Glahn A, Buddensiek N, et al. Lateral frontal cortex volume reduction in Tourette syndrome revealed by VBM. BMC Neurosci 2012;13:17. [18] Bohlhalter S, Goldfine A, Matteson S, Garraux G, Hanakawa T, Kansaku K, et al. Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study. Brain 2006;129:2029–37. [19] Neuner I, Schneider F, Shah NJ. Functional neuroanatomy of tics. Int Rev Neurobiol 2013;112:35–71.
Christos Ganos Department of Neurology, University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany Sobell Department of Motor Neuroscience and Movement Disorders, University College London Institute of Neurology, London, United Kingdom Department of Paediatric and Adult Movement Disorders and Neuropsychiatry, Institute of Neurogenetics, University of Lübeck, Germany Corresponding author at: Sobell Department ofMotor Neuroscience and Movement Disorders, UCL Institute of Neurology, Queen Square, London WC1N 3BG, United Kingdom. E-mail addresses: [email protected]. Simone Kühn Center for Lifespan Psychology, Max Planck Institute for Human Development, Lentzeallee 94, 14195 Berlin, Germany
488
Letters to the Editor
Patrick Haggard Institute of Cognitive Neuroscience, University College London, United Kingdom Alexander Münchau Department of Paediatric and Adult Movement Disorders and Neuropsychiatry, Institute of Neurogenetics, University of Lübeck, Germany 20 March 2014
DOI of original article: http://dx.doi.org/10.1016/j.jpsychores.2014.03.009 http://dx.doi.org/10.1016/j.jpsychores.2014.03.012 0022 – 3999/$ – see front matter © 2014 Elsevier Inc. All rights reserved.
487
of voluntary action might be related to the presence of involuntary hyperkinesias is risky. Although distinct areas involved in voluntary action generation and action inhibition might be implicated in the pathogenesis of tics [18,19], channelling results from different studies exploring hyperkinesias of different aetiologies to common pathophysiological pathways carries the danger of oversimplification. Combining hypothesis-driven multimodal approaches in different clinical populations studied longitudinally will promote understanding of the delicate balance between involuntary movements and voluntary motor control. References
Antonio Cerasa UOS-IBFM, National Research Council, Catanzaro, Italy Corresponding author at: Consiglio Nazionale delle Ricerche (CNR), Unità di Ricerca Neuroimmagini, Catanzaro, 88100, Italy. Tel.: +39 0961 369 5904. E-mail addresses: [email protected]. Aldo Quattrone UOS-IBFM, National Research Council, Catanzaro, Italy Institute of Neurology, University “Magna Graecia”, Germaneto, CZ, Italy 18 February 2014
DOI of original article: http://dx.doi.org/10.1016/j.jpsychores.2013.10.014 http://dx.doi.org/10.1016/j.jpsychores.2014.03.009 0022 – 3999/$ – see front matter © 2014 Elsevier Inc. All rights reserved.
Reply to: The role of the inferior frontal cortex in hyperkinetic movement disorders
Sir, Gilles de la Tourette syndrome (GTS) is a neurodevelopmental disorder. Tics resemble normal motor behaviour, appearing uncontrollable and out of context. Tic production has been linked to either excess generation of movement, insufficient motor inhibition, or both [1]. Neuropathological studies of inhibitory interneuronal populations predominantly from sensorimotor parts of the striatum [2,3], as well as recordings of neuronal activity from animal models of tics and GTS patients have provided converging evidence that tics might indeed be excessively generated due to local disinhibition at subcortical levels [4–7]. However, the translation of these results to a general inhibitory deficit of motor behaviour, for example in inhibition of voluntary actions can be precarious. Several studies have demonstrated that GTS patients of different ages have normal action inhibition (i.e. commission errors) in Stop Signal Reaction Time (SSRT) and Go/NoGo tasks [8–10]. Also, some studies have suggested that GTS patients might in fact have enhanced control over their motor output, as an adaptation to having to suppress tics in different social situations over the years [11–13]. We showed that the ability to inhibit tics on demand does not correlate with grey matter volumes of the right inferior frontal cortex and left frontal pole. Nevertheless, grey matter volume in these areas was reduced compared to healthy controls [14]. This further confirms previous findings in adult GTS patients demonstrating decreased cortical volumes [15–17]. We suggest that grey matter volume reductions might represent trait characteristics of tic persistence into adulthood. In contrast, inhibition of tics on demand should be considered a state characteristic of behavioural motor performance. The assumption that brain structure corresponds in a one to one fashion to function and behavioural performance may be unwarranted. Also, the speculation that behavioural deficits in the inhibition
[1] Ganos C, Roessner V, Munchau A. The functional anatomy of Gilles de la Tourette syndrome. Neurosci Biobehav Rev 2013;37:1050–62. [2] Kalanithi PS, Zheng W, Kataoka Y, DiFiglia M, Grantz H, Saper CB, et al. Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc Natl Acad Sci U S A 2005;102:13307–12. [3] Kataoka Y, Kalanithi PS, Grantz H, Schwartz ML, Saper C, Leckman JF, et al. Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome. J Comp Neurol 2010;518:277–91. [4] Bronfeld M, Bar-Gad I. Tic disorders: what happens in the basal ganglia? Neuroscientist 2013;19:101–8. [5] Bronfeld M, Belelovsky K, Bar-Gad I. Spatial and temporal properties of tic-related neuronal activity in the cortico-basal ganglia loop. J Neurosci 2011;31:8713–21. [6] McCairn KW, Bronfeld M, Belelovsky K, Bar-Gad I. The neurophysiological correlates of motor tics following focal striatal disinhibition. Brain 2009;132:2125–38. [7] Zhuang P, Hallett M, Zhang X, Li J, Zhang Y, Li Y. Neuronal activity in the globus pallidus internus in patients with tics. J Neurol Neurosurg Psychiatry 2009;80:1075–81. [8] Roessner V, Albrecht B, Dechent P, Baudewig J, Rothenberger A. Normal response inhibition in boys with Tourette syndrome. Behav Brain Funct 2008;4:29. [9] Serrien DJ, Orth M, Evans AH, Lees AJ, Brown P. Motor inhibition in patients with Gilles de la Tourette syndrome: functional activation patterns as revealed by EEG coherence. Brain 2005;128:116–25. [10] Watkins LH, Sahakian BJ, Robertson MM, Veale DM, Rogers RD, Pickard KM, et al. Executive function in Tourette's syndrome and obsessive–compulsive disorder. Psychol Med 2005;35:571–82. [11] Jackson GM, Mueller SC, Hambleton K, Hollis CP. Enhanced cognitive control in Tourette syndrome during task uncertainty. Exp Brain Res 2007;182:357–64. [12] Jackson SR, Parkinson A, Jung J, Ryan SE, Morgan PS, Hollis C, et al. Compensatory neural reorganization in Tourette syndrome. Curr Biol 2011;21:580–5. [13] Mueller SC, Jackson GM, Dhalla R, Datsopoulos S, Hollis CP. Enhanced cognitive control in young people with Tourette's syndrome. Curr Biol 2006;16:570–3. [14] Ganos C, Kuhn S, Kahl U, Schunke O, Brandt V, Baumer T, et al. Prefrontal cortex volume reductions and tic inhibition are unrelated in uncomplicated GTS adults. J Psychosom Res 2014;76:84–7. [15] Draganski B, Martino D, Cavanna AE, Hutton C, Orth M, Robertson MM, et al. Multispectral brain morphometry in Tourette syndrome persisting into adulthood. Brain 2010;133:3661–75. [16] Muller-Vahl KR, Kaufmann J, Grosskreutz J, Dengler R, Emrich HM, Peschel T. Prefrontal and anterior cingulate cortex abnormalities in Tourette syndrome: evidence from voxel-based morphometry and magnetization transfer imaging. BMC Neurosci 2009;10:47. [17] Wittfoth M, Bornmann S, Peschel T, Grosskreutz J, Glahn A, Buddensiek N, et al. Lateral frontal cortex volume reduction in Tourette syndrome revealed by VBM. BMC Neurosci 2012;13:17. [18] Bohlhalter S, Goldfine A, Matteson S, Garraux G, Hanakawa T, Kansaku K, et al. Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study. Brain 2006;129:2029–37. [19] Neuner I, Schneider F, Shah NJ. Functional neuroanatomy of tics. Int Rev Neurobiol 2013;112:35–71.
Christos Ganos Department of Neurology, University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany Sobell Department of Motor Neuroscience and Movement Disorders, University College London Institute of Neurology, London, United Kingdom Department of Paediatric and Adult Movement Disorders and Neuropsychiatry, Institute of Neurogenetics, University of Lübeck, Germany Corresponding author at: Sobell Department ofMotor Neuroscience and Movement Disorders, UCL Institute of Neurology, Queen Square, London WC1N 3BG, United Kingdom. E-mail addresses: [email protected]. Simone Kühn Center for Lifespan Psychology, Max Planck Institute for Human Development, Lentzeallee 94, 14195 Berlin, Germany
488
Letters to the Editor
Patrick Haggard Institute of Cognitive Neuroscience, University College London, United Kingdom Alexander Münchau Department of Paediatric and Adult Movement Disorders and Neuropsychiatry, Institute of Neurogenetics, University of Lübeck, Germany 20 March 2014
DOI of original article: http://dx.doi.org/10.1016/j.jpsychores.2014.03.009 http://dx.doi.org/10.1016/j.jpsychores.2014.03.012 0022 – 3999/$ – see front matter © 2014 Elsevier Inc. All rights reserved.
