Abstract
Progressive supranuclear palsy (PSP) is the most common atypical parkinsonian syndrome and an important differential diagnosis of parkinson’s disease (PD). The clinical diagnosis of PSP relies on characteristic symptoms. There is evidence of clinical subgroups within the entity of PSP interfering with making the firm diagnosis. It was the aim of the study to clarify the differences between phenotypical subtypes of PSP and PD focusing on transcallosal inhibition (TI). A systematic chart review of 67 patients supposed to have probable PSP was done in a standardized diagnostic work-up. As only complete data sets were included into further analysis, 26 PSP patients (mean age 68.6 ± 7.1 years) could be evaluated and subdivided into Richardson’s syndrome (RS) (n = 15) or PSP of parkinsonian type (PSP-P) (n = 11). Fifteen PD patients served as controls. TI was evaluated by investigation of the ipsilateral silent period (iSP) with transcranial magnetic stimulation (TMS). Cognition was assessed by the Addenbrooke′s cognitive examination (ACE-R). TMS revealed a significantly more severe affection of TI in RS patients as compared to PSP-P and PD patients who showed similar neurophysiological findings. 47 % of RS patient displayed an iSP loss, whereas PSP-P and PD did not. There was a significant correlation between iSP latency and ACE-R (Spearman’s coefficient −0.369, P = 0.010). In conclusion, RS patients—contrary to PSP-P and PD patients—had pathological TI at least in one hemisphere indicating more severe involvement of transcallosally projecting output neurons in RS.
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Bäumer T, Pramstaller PP, Siebner HR, Schippling S, Hagenah J, Peller M, Gerloff C, Klein C, Münchau A (2007) Sensorimotor integration is abnormal in asymptomatic parkin mutation carriers: a TMS study. Neurology 69:1976–1981
Buhmann C, Gorsler A, Bäumer T, Hidding U, Demiralay C, Hinkelmann K, Weiller C, Sie’ber HR, Münchau A (2004) Abnormal excitability of premotor-motor connections in de novo parkinson’s disease. Brain 127:2732–2746
Canu E, Agosta F, Baglio F, Galantucci S, Nemni R, Filippi M (2011) Diffusion tensor magnetic resonance imaging tractography in progressive supranuclear palsy. Mov Disord 26:1752–1755
Classen J, Steinfelder B, Liepert et al (2000) Cutaneomotor integration is somatotopically organized at various levels of the central nervous system and task dependent. Exp Brain Res 130:48–59
Eusebio A, Azulay JP, Witjas T, Rico A, Attarian S (2007) Assessment of cortico-spinal tract impairment in multiple system atrophy using transcranial magnetic stimulation. Clin Neurophysiol 118:815–823
Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184
Karnik NS, D`Apuzzo M, Greicius M (2006) Non-fluent progressive aphsia, depression, and OCD in a woman with progressive supranuclear palsy: neuroanatomical and neuropathological correlations. Neurocase 12:332–338
Khedr M, Ahmed MA, Darwish ES, Ali AM (2011) The relationship between motor cortex excitability and severity of Alzheimer′s disease: a transcranial magnetic stimulation study. Neurophysiol Clin 41:107–113
Koch G (2010) Repetitive transcranial magnetic stimulation: a tool for human cerebellar plasticity. Funct Neurol 25:159–163
Kühn A, Grosse P, Holtz K, Brown P, Meyer BU, Kupsch A (2004) Patterns of abnormal motor cortex excitability in atypical parkinsonian syndromes. Clin Neurophysiol 115:1786–1795
Leh SE, Petrides M, Strafella AP (2010) The neural circuitry of executive functions in healthy subjects and parkinson′s disease. Neuropharmacology 35:70–85
Litvan I (2004) Update on progressive supranuclear palsy. Curr Neurol Neurosci Rep 4:296–302
Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jancovic J, Quinn NP, Tolosa E, Zee DS (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome): report of the NINDS-SPSP International workshop. Neurology 47:1–9
Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR (2006) The Addenbrooke′s cognitive examination revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry 21:1078–1085
Mir P, Matsunaga K, Gilio F, Quinn NP, Siebner HR, Rothwell JC (2005) Dopaminergic drugs restore facilitatory premotor–motor interactions in Parkinson disease. Neurology 64:1906–1912
Mochizuki A, Ueda Y, Komatsuzaki Y, Tsuchiya K, Arai T, Shoji S (2003) Progressive supranuclear palsy presenting with primary progressive aphasia—clinicopathological report of an autopsy case. Acta Neuropathol 105:610–614
Morita Y, Osaki Y, Doi Y (2008) Transcranial magnetic stimulation for differential diagnosis in patients with parkinsonism. Acta Neurol Scand 118:159–163
Nardone R, Florio I, Lochner P, Tezzon F (2005) Cholinergic cortical circuits in Parkinson’s disease and in progressive supranuclear palsy: a transcranial magnetic stimulation study. Exp Brain Res 163:128–131
Oba H, Yagishita A, Terada H, Barkovich AJ, Kutomi K, Yamauchi T, Furui S, Shimizu T, Uchigata M, Matsumura K, Sonoo M, Sakai M, Takada K, Harasawa A, Takeshita K, Kohtake H, Tanaka H, Suzuki S (2005) New and reliable MRI diagnosis for progressive supranuclear palsy. Neurology 64:2050–2055
Osaki Y, Ben-Shlomo Y, Lees AJ, Daniel SE, Colosimo C, Wenning G, Quinn N (2004) Accuracy of clinical diagnosis of progressive supranuclear palsy. Mov Disord 19:181–189
Payan CAM, Viallet F, Landwehrmeyer BG, Bonnet AM, Borg M, Durif F, Lacomblez L, Bloch F, Verny M, Fermian J, Agiid Y, Ludolph AC, Leigh PN, Bensimon G, on behalf oft he NNIPPS Study Group (2011) Disease severity and progression in progressive supranuclear palsy and multi system atrophy: validation of the NNIPPS-PARKINSON PLUS SCALE. PLOS One 6:e22293
Roick H, von Giesen HJ, Benecke R (1993) On the origin of the postexcitatory inhibition seen after transcranial magnetic stimulation in awake human subjects. Exp Brain Res 94:489–498
Scaravilli T, Tolosa E, Ferrer I (2005) Progressive supranuclear palsy and corticobasal degeneration: lumping versus splitting. Mov Disord 20:S21–S28
Shirota Y, Hamada M, Hanajima R, Terao Y, Matsumoto H, Ohminami S, Tsuji S, Ugawa Y (2010) Cerebellar dysfunction in progressive supranuclear palsy: a transcranial magnetic stimulation study. Mov Disord 25:2413–2419
Siebner HR, Rossmeier C, Mentschel C, Peinemann A, Conrad B (2000) Short-term motor improvement after subthreshold 5-Hz repetitive transcranial magnetic stimulation of the primary motor hand area in Parkinson′s disease. J Neurol Sci 178:91–94
Stamelou M, Knake S, Oertel WH, Höglinger GU (2011) Magnetic resonance imaging in progressive supranuclear palsy. J Neurol 258:549–558
Suppa A, Lezzi E, Conte A, Belvisi D, Marsili L, Modugno N, Fabbrini G, Berardelli A (2010) Dopamine influences primary motor cortex plasticity and dorsal premotor-to-motor connectivity in parkinson′s disease. 20:2224–2233
Walter U, Dressler D, Probst T, Wolters A, Abu-Mugheisib M, Wittstock M, Benecke R (2007) Transcranial brain sonography findings in discriminating between parkinsonism and idiopathic Parkinson disease. Arch Neurol 64:1635–1640
Wang J, Wai Y, Lin WY, Ng S, Wang CH, Hsieh R, Hsiegh C, Chen RS, Lu CS (2010) Microstructural changes in patients with progressive supranuclear palsy: a diffusion tensor imaging study. J Magn Reson Imaging 32:69–75
Warmuth-Metz M, Naumann M, Csoti I, Solymosi L (2001) Measurement of the midbrain diameter on routine magnetic resonance imaging. Arch Neurol 58:1076–1079
Whitwell JL, Master AV, Avula R, Kantarci K, Eggers SD, Edmonson HA, Jack CR Jr, Josephs KA (2011) Clinical correlates of white matter tract degeneration in progressive supranuclear palsy. Arch Neurol 68:753–760
Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L, Holton JL, Revesz T, Lees AJ (2005) Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 128:1247–1258
Williams DR, Holton JL, Strand K, Revesz T, Lees AJ (2007) Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord 22:2235–2241
Wittstock M, Wolters A, Benecke R (2007) Transcallosal inhibition in amyotrophic lateral sclerosis. Clin Neurophysiol 118:301–307
Wolters A, Classen J, Kunesch E, Grossmann A, Benecke R (2004) Measurement of transcallosally mediated cortical inhibition for differentiating parkinsonian syndromes. Mov Disord 19:518–528
Ziemann U, Bruns D, Paulus W (1996) Enhancement of human cortex inhibition by the dopamine receptor agonist pergolide: evidence from transcranial magnetic stimulation. Neurosci Lett 2008:187–190
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Wittstock, M., Pohley, I., Walter, U. et al. Interhemispheric inhibition in different phenotypes of progressive supranuclear palsy. J Neural Transm 120, 453–461 (2013). https://doi.org/10.1007/s00702-012-0879-7
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DOI: https://doi.org/10.1007/s00702-012-0879-7