- Email: [email protected]
The role of the inferior frontal cortex in hyperkinetic movement disorders
486
Letters to the Editor
[9] Green BL, Rowland JH, Krupnick JL, et al. Prevalence of posttraumatic stress disorder in women with breast cancer. Psychosomatics 1998;39:102–11. [10] Widows MR, Jacobsen PB, Fields KK. Relation of psychological vulnerability factors to posttraumatic stress disorder symptomatology in bone marrow transplant recipients. Psychosom Med 2000;62:873–82. [11] Kessler RC, Chiu WT, Demler O, et al. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 2005;62:617–27.
Linda Kwakkenbos Department of Psychiatry, McGill University, Montréal, Québec, Canada Lady Davis Institute for Medical Research, Jewish General Hospital, Montréal, Québec, CanadaCorresponding author at: Jewish General Hospital; 4333 Cote Ste Catherine Road; Montreal, Quebec H3T 1E4. Tel.: +1 514 340 8222x8578. E-mail addresses: [email protected] James C Coyne University of Groningen, Groningen, the Netherlands Institute for Health, Health Care Policy and Aging Research, Rutgers University, USA Brett D Thombs Department of Psychiatry, McGill University, Montréal, Québec, Canada Lady Davis Institute for Medical Research, Jewish General Hospital, Montréal, Québec, Canada Department of Medicine (Division of Rheumatology), McGill University, Montréal, Québec, Canada Epidemiology, Biostatistics, and Occupational Health, McGill University, Montréal, Québec, Canada Educational and Counselling Psychology, McGill University, Montréal, Québec, Canada School of Nursing, McGill University, Montréal, Québec, Canada 24 March 2014 http://dx.doi.org/10.1016/j.jpsychores.2014.03.103 0022 – 3999/$ – see front matter © 2014 Elsevier Inc. All rights reserved.
The role of the inferior frontal cortex in hyperkinetic movement disorders
dystonia and Huntington's disease, are caused by maladaptive synaptic plasticity that can be expressed by functional changes such as an increase in transmitter release, receptor regulation and synaptic plasticity or anatomical modifications such as axonal regeneration, sprouting, synaptogenesis and neurogenesis. With this in mind, one may suppose similar neurodegenerative mechanisms underlying pathophysiological processes of GTS. Considering, PD patients, the development of LIDs has been attributed to dysfunctional brain plasticity triggered by the combined effects of dopamine denervation and chronic pharmacological dopamine replacement [7]. Our recent neuroimaging studies have shed new light on the pathophysiological mechanisms underlying LIDs [8]. Indeed, we demonstrated that these patients are characterised by abnormal grey matter volume in the IFC. This finding has been confirmed using different population [9] and neuroimaging metrics [10], and has already raised an interesting scientific debate on the toxic effects of levodopa on brain morphometry [11]. Interesting, similar evidence highlighting the presence of neural abnormalities in the IFC, has also been provided in psychiatric realm: TDs. Originally, the term TDs referred to abnormal movements produced by long-term dopamine receptor antagonist therapy, mainly characterised by rapid, repetitive, stereotypic movements affecting mainly the oral, buccal and lingual areas and less the limb and the trunk. A recent neuroimaging study [12] investigating the neuroanatomical differences between schizophrenic patients with TDs with respect to patients without TDs (closely matched for age at onset of illness, duration of illness, or antipsychotic chlorpromazine equivalent dose) demonstrated the presence of volumetric abnormalities in the same prefrontal region described in LIDs patients. The merit of this work [12] was to demonstrate that chronic psychotropic treatment in schizophrenic patients might result in maladaptive neural rearrangements. To establish whether IFC neural abnormalities detected in GTS, LIDs and TDs have a causative effect (or whether this might be only considered as a consequence of having hyperkinetic movements for a long time) represents an exciting new challenge for future studies. We retain that studies designed to stimulate this region could become more useful. Indeed, the effectiveness (or non-effectiveness) of the repetitive transcranial stimulation (rTMS) over the IFC can help us to refute this hypothesis, as well as to provide a possible therapeutic target for improving motor disorders, as already proposed by our group on PD patients with LIDs [13]. Conflict of interest
To the Editor: We read with interest the article by Ganos et al., Prefrontal cortex volume reductions and tic inhibition are unrelated in uncomplicated GTS adults. J Psychosom Res. 2014; 76: 84-7 [1] who, upon investigation of the neural basis of Tics in Gilles de la Tourette syndrome (GTS), demonstrated the presence of anatomical abnormalities in a specific frontal region, the right inferior frontal cortex (IFC), which was unrelated to clinical symptoms. The IFC is part of a well-known neural network involved in response inhibition [2]. Previous functional magnetic resonance imaging (fMRI) studies have demonstrated that this network is fundamentally right-lateralised and comprised of: the IFC, supplementary motor areas, primary motor cortex, subthalamic nucleus and striatum [2,3]. The fact that GTS patients are associated with anatomical changes in the IFC might stimulate an exciting hypothesis. Indeed, the same pattern of neural abnormalities has been also described in other hyperkinetic movement disorders: in Parkinson's disease (PD) patients with levodopa-induced dyskinesias (LIDs) and schizophrenic patients affected by tardive dyskinesias (TDs). In the last years, several influential authors [4–6] proposed that some hyperkinetic movement disorders, in the neurological and psychiatric realms, such as: LIDs, TDs, primary
The authors declare no conflicts of interest. References [1] Ganos C, Kühn S, Kahl U, Schunke O, Brandt V, Bäumer T, et al. Prefrontal cortex volume reductions and tic inhibition are unrelated in uncomplicated GTS adults. J Psychosom Res 2014;76:84–7. [2] Aron AR, Poldrack RA. Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 2006;26:2424e33. [3] King AV, Linke J, Gass A, Hennerici MG, Tost H, Poupon C, et al. Microstructure of a three-way anatomical network predicts individual differences in response inhibition: a tractography study. Neuroimage 2012;59:1949–59. [4] Breakefield XO, Blood AJ, Li Y, Hallett M, Hanson PI, Standaert DG. The pathophysiological basis of dystonias. Nat Rev Neurosci 2008;9:222–34. [5] Teo JT, Edwards MJ, Bhatia K. Tardive dyskinesia is caused by maladaptive synaptic plasticity: a hypothesis. Mov Disord 2012;27:1205–15. [6] Cenci MA. Dopamine dysregulation of movement control in L-DOPA-induced dyskinesia. Trends Neurosci 2007;30:236–43. [7] Calabresi P, Giacomini P, Centonze D, Bernardi G. Levodopa-induced dyskinesia: a pathological form of striatal synaptic plasticity? Ann Neurol 2000;47:S60–8. [8] Cerasa A, Pugliese P, Messina D, Morelli M, Gioia MC, Salsone M, et al. Prefrontal alterations in Parkinson's disease with levodopa-induced dyskinesia during fMRI motor task. Mov Disord 2012;27:364–71. [9] Cerasa A, Salsone M, Morelli M, Pugliese P, Arabia G, Gioia MC, et al. Age at onset influences neurodegenerative processes underlying PD with levodopa-induced dyskinesias. Parkinsonism Relat Disord 2013;19:883–8.
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.
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
Letters to the Editor
[9] Green BL, Rowland JH, Krupnick JL, et al. Prevalence of posttraumatic stress disorder in women with breast cancer. Psychosomatics 1998;39:102–11. [10] Widows MR, Jacobsen PB, Fields KK. Relation of psychological vulnerability factors to posttraumatic stress disorder symptomatology in bone marrow transplant recipients. Psychosom Med 2000;62:873–82. [11] Kessler RC, Chiu WT, Demler O, et al. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 2005;62:617–27.
Linda Kwakkenbos Department of Psychiatry, McGill University, Montréal, Québec, Canada Lady Davis Institute for Medical Research, Jewish General Hospital, Montréal, Québec, CanadaCorresponding author at: Jewish General Hospital; 4333 Cote Ste Catherine Road; Montreal, Quebec H3T 1E4. Tel.: +1 514 340 8222x8578. E-mail addresses: [email protected] James C Coyne University of Groningen, Groningen, the Netherlands Institute for Health, Health Care Policy and Aging Research, Rutgers University, USA Brett D Thombs Department of Psychiatry, McGill University, Montréal, Québec, Canada Lady Davis Institute for Medical Research, Jewish General Hospital, Montréal, Québec, Canada Department of Medicine (Division of Rheumatology), McGill University, Montréal, Québec, Canada Epidemiology, Biostatistics, and Occupational Health, McGill University, Montréal, Québec, Canada Educational and Counselling Psychology, McGill University, Montréal, Québec, Canada School of Nursing, McGill University, Montréal, Québec, Canada 24 March 2014 http://dx.doi.org/10.1016/j.jpsychores.2014.03.103 0022 – 3999/$ – see front matter © 2014 Elsevier Inc. All rights reserved.
The role of the inferior frontal cortex in hyperkinetic movement disorders
dystonia and Huntington's disease, are caused by maladaptive synaptic plasticity that can be expressed by functional changes such as an increase in transmitter release, receptor regulation and synaptic plasticity or anatomical modifications such as axonal regeneration, sprouting, synaptogenesis and neurogenesis. With this in mind, one may suppose similar neurodegenerative mechanisms underlying pathophysiological processes of GTS. Considering, PD patients, the development of LIDs has been attributed to dysfunctional brain plasticity triggered by the combined effects of dopamine denervation and chronic pharmacological dopamine replacement [7]. Our recent neuroimaging studies have shed new light on the pathophysiological mechanisms underlying LIDs [8]. Indeed, we demonstrated that these patients are characterised by abnormal grey matter volume in the IFC. This finding has been confirmed using different population [9] and neuroimaging metrics [10], and has already raised an interesting scientific debate on the toxic effects of levodopa on brain morphometry [11]. Interesting, similar evidence highlighting the presence of neural abnormalities in the IFC, has also been provided in psychiatric realm: TDs. Originally, the term TDs referred to abnormal movements produced by long-term dopamine receptor antagonist therapy, mainly characterised by rapid, repetitive, stereotypic movements affecting mainly the oral, buccal and lingual areas and less the limb and the trunk. A recent neuroimaging study [12] investigating the neuroanatomical differences between schizophrenic patients with TDs with respect to patients without TDs (closely matched for age at onset of illness, duration of illness, or antipsychotic chlorpromazine equivalent dose) demonstrated the presence of volumetric abnormalities in the same prefrontal region described in LIDs patients. The merit of this work [12] was to demonstrate that chronic psychotropic treatment in schizophrenic patients might result in maladaptive neural rearrangements. To establish whether IFC neural abnormalities detected in GTS, LIDs and TDs have a causative effect (or whether this might be only considered as a consequence of having hyperkinetic movements for a long time) represents an exciting new challenge for future studies. We retain that studies designed to stimulate this region could become more useful. Indeed, the effectiveness (or non-effectiveness) of the repetitive transcranial stimulation (rTMS) over the IFC can help us to refute this hypothesis, as well as to provide a possible therapeutic target for improving motor disorders, as already proposed by our group on PD patients with LIDs [13]. Conflict of interest
To the Editor: We read with interest the article by Ganos et al., Prefrontal cortex volume reductions and tic inhibition are unrelated in uncomplicated GTS adults. J Psychosom Res. 2014; 76: 84-7 [1] who, upon investigation of the neural basis of Tics in Gilles de la Tourette syndrome (GTS), demonstrated the presence of anatomical abnormalities in a specific frontal region, the right inferior frontal cortex (IFC), which was unrelated to clinical symptoms. The IFC is part of a well-known neural network involved in response inhibition [2]. Previous functional magnetic resonance imaging (fMRI) studies have demonstrated that this network is fundamentally right-lateralised and comprised of: the IFC, supplementary motor areas, primary motor cortex, subthalamic nucleus and striatum [2,3]. The fact that GTS patients are associated with anatomical changes in the IFC might stimulate an exciting hypothesis. Indeed, the same pattern of neural abnormalities has been also described in other hyperkinetic movement disorders: in Parkinson's disease (PD) patients with levodopa-induced dyskinesias (LIDs) and schizophrenic patients affected by tardive dyskinesias (TDs). In the last years, several influential authors [4–6] proposed that some hyperkinetic movement disorders, in the neurological and psychiatric realms, such as: LIDs, TDs, primary
The authors declare no conflicts of interest. References [1] Ganos C, Kühn S, Kahl U, Schunke O, Brandt V, Bäumer T, et al. Prefrontal cortex volume reductions and tic inhibition are unrelated in uncomplicated GTS adults. J Psychosom Res 2014;76:84–7. [2] Aron AR, Poldrack RA. Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 2006;26:2424e33. [3] King AV, Linke J, Gass A, Hennerici MG, Tost H, Poupon C, et al. Microstructure of a three-way anatomical network predicts individual differences in response inhibition: a tractography study. Neuroimage 2012;59:1949–59. [4] Breakefield XO, Blood AJ, Li Y, Hallett M, Hanson PI, Standaert DG. The pathophysiological basis of dystonias. Nat Rev Neurosci 2008;9:222–34. [5] Teo JT, Edwards MJ, Bhatia K. Tardive dyskinesia is caused by maladaptive synaptic plasticity: a hypothesis. Mov Disord 2012;27:1205–15. [6] Cenci MA. Dopamine dysregulation of movement control in L-DOPA-induced dyskinesia. Trends Neurosci 2007;30:236–43. [7] Calabresi P, Giacomini P, Centonze D, Bernardi G. Levodopa-induced dyskinesia: a pathological form of striatal synaptic plasticity? Ann Neurol 2000;47:S60–8. [8] Cerasa A, Pugliese P, Messina D, Morelli M, Gioia MC, Salsone M, et al. Prefrontal alterations in Parkinson's disease with levodopa-induced dyskinesia during fMRI motor task. Mov Disord 2012;27:364–71. [9] Cerasa A, Salsone M, Morelli M, Pugliese P, Arabia G, Gioia MC, et al. Age at onset influences neurodegenerative processes underlying PD with levodopa-induced dyskinesias. Parkinsonism Relat Disord 2013;19:883–8.
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.
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