Skip to main content
Top
Published in: Neuroradiology 3/2012

01-03-2012 | Functional Neuroradiology

Hypoactivation of the primary sensorimotor cortex in de novo Parkinson’s disease

A motor fMRI study under controlled conditions

Authors: Carlo Tessa, Claudio Lucetti, Stefano Diciotti, Lorenzo Paoli, Paolo Cecchi, Marco Giannelli, Filippo Baldacci, Andrea Ginestroni, Claudio Vignali, Mario Mascalchi, Ubaldo Bonuccelli

Published in: Neuroradiology | Issue 3/2012

Login to get access

Abstract

Introduction

Nuclear medicine studies in Parkinson’s disease (PD) indicate that nigrostriatal damage causes a widespread cortical hypoactivity assumed to be due to reduced excitatory thalamic outflow. However, so far, functional MRI (fMRI) studies have provided controversial data about this “functional deafferentation” phenomenon. To further clarify this issue, we assessed, with fMRI, de novo drug-naive PD patients using a relatively complex motor task under strictly controlled conditions.

Methods

Nineteen de novo PD patients with right-predominant or bilateral symptoms and 13 age-matched healthy volunteers performed continuous writing of “8” figures with the right-dominant hand using a MR-compatible device that enables identification of incorrectly performed tasks and measures the size and the frequency of the “8”s. The data were analyzed with FSL software and correlated with the clinical severity rated according to the Hoehn and Yahr (HY) staging system.

Results

Fifteen (89%) of 19 PD patients and 12 (92%) of 13 controls correctly executed the task. PD patients showed significant hypoactivation of the left primary sensorimotor cortex (SM1) and cerebellum and no hyperactive areas as compared to controls. However, activation in SM1 and supplementary motor area bilaterally, in left supramarginal, parietal inferior, parietal superior and frontal superior gyri as well as in right parietal superior and angular gyri paralleled increasing disease severity as assessed with the HY stage.

Conclusions

In line with the “deafferentation hypothesis”, fMRI demonstrates hypoactivation of the SM1 in the early clinical stage of PD.
Appendix
Available only for authorised users
Literature
1.
go back to reference Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375PubMedCrossRef Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375PubMedCrossRef
2.
go back to reference Rascol O, Sabatini U, Chollet F, Celsis P, Montastruc JL, Marc-Vergnes JP, Rascol A (1992) Supplementary and primary sensory motor area activity in Parkinson’s disease. Regional cerebral blood flow changes during finger movements and effects of apomorphine. Arch Neurol 49:144–148PubMedCrossRef Rascol O, Sabatini U, Chollet F, Celsis P, Montastruc JL, Marc-Vergnes JP, Rascol A (1992) Supplementary and primary sensory motor area activity in Parkinson’s disease. Regional cerebral blood flow changes during finger movements and effects of apomorphine. Arch Neurol 49:144–148PubMedCrossRef
3.
go back to reference Jenkins IH, Fernandez W, Playford ED, Lees AJ, Frackowiak RS, Passingham RE, Brooks DJ (1992) Impaired activation of the supplementary motor area in Parkinson’s disease is reversed when akinesia is treated with apomorphine. Ann Neurol 32:749–757PubMedCrossRef Jenkins IH, Fernandez W, Playford ED, Lees AJ, Frackowiak RS, Passingham RE, Brooks DJ (1992) Impaired activation of the supplementary motor area in Parkinson’s disease is reversed when akinesia is treated with apomorphine. Ann Neurol 32:749–757PubMedCrossRef
4.
go back to reference Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RS, Brooks DJ (1992) Impaired mesial frontal and putamen activation in Parkinson’s disease: a positron emission tomography study. Ann Neurol 32:151–161PubMedCrossRef Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RS, Brooks DJ (1992) Impaired mesial frontal and putamen activation in Parkinson’s disease: a positron emission tomography study. Ann Neurol 32:151–161PubMedCrossRef
5.
go back to reference Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118:913–933PubMedCrossRef Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118:913–933PubMedCrossRef
6.
go back to reference Samuel M, Ceballos Baumann AO, Turjanski N, Boecker H, Gorospe A, Linazasoro G, Holmes AP, DeLong MR, Vitek JL, Thomas DG, Quinn NP, Obeso JA, Brooks DJ (1997) Pallidotomy in Parkinson’s disease increases supplementary motor area and prefrontal activation during performance of volitional movements. An H2O PET study. Brain 120:1301–1313PubMedCrossRef Samuel M, Ceballos Baumann AO, Turjanski N, Boecker H, Gorospe A, Linazasoro G, Holmes AP, DeLong MR, Vitek JL, Thomas DG, Quinn NP, Obeso JA, Brooks DJ (1997) Pallidotomy in Parkinson’s disease increases supplementary motor area and prefrontal activation during performance of volitional movements. An H2O PET study. Brain 120:1301–1313PubMedCrossRef
7.
go back to reference Eckert T, Tang C, Eidelberg D (2007) Assessing the progression of Parkinson’s disease: a metabolic network approach. Lancet Neurol 6:926–932PubMedCrossRef Eckert T, Tang C, Eidelberg D (2007) Assessing the progression of Parkinson’s disease: a metabolic network approach. Lancet Neurol 6:926–932PubMedCrossRef
8.
go back to reference Teune LK, Bartels AL, De Jong BM, Willemsen AT, Eshuis SA, de Vries JJ, van Oostrom JC, Leenders KL (2010) Typical cerebral metabolic patterns in neurodegenerative brain diseases. Mov Disord 25:2395–2404PubMedCrossRef Teune LK, Bartels AL, De Jong BM, Willemsen AT, Eshuis SA, de Vries JJ, van Oostrom JC, Leenders KL (2010) Typical cerebral metabolic patterns in neurodegenerative brain diseases. Mov Disord 25:2395–2404PubMedCrossRef
9.
go back to reference Limousin P, Greens J, Pollak P, Rothwell J, Bernabid AL, Frackowiak R (1997) Changes in cerebral activity pattern due to subthalamic nuckeus or internal pallidum stimulation in Parkinson’s disease. Ann Neurol 42:283–291PubMedCrossRef Limousin P, Greens J, Pollak P, Rothwell J, Bernabid AL, Frackowiak R (1997) Changes in cerebral activity pattern due to subthalamic nuckeus or internal pallidum stimulation in Parkinson’s disease. Ann Neurol 42:283–291PubMedCrossRef
10.
go back to reference Ceballos-Baumann AO, Boecker H, Bartestenstein P, von Falkenhayn I, Riescher H, Conrad B, Moringlane JR, Alesch F (1999) A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 56:997–1003PubMedCrossRef Ceballos-Baumann AO, Boecker H, Bartestenstein P, von Falkenhayn I, Riescher H, Conrad B, Moringlane JR, Alesch F (1999) A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 56:997–1003PubMedCrossRef
11.
go back to reference Strafella AP, Dagher A, Sadikot AF (2003) Cerebral blood flow changes induced by subthalamic stimulation in Parkinson’s disease. Neurology 60:1039–1042PubMed Strafella AP, Dagher A, Sadikot AF (2003) Cerebral blood flow changes induced by subthalamic stimulation in Parkinson’s disease. Neurology 60:1039–1042PubMed
12.
go back to reference Buhmann C, Glauche V, Sturenburg HJ, Oechsner M, Weiller C, Buchel C (2003) Pharmacologically modulated fMRI cortical responsiveness to levodopa in drug-naive hemiparkinsonian patients. Brain 126:451–461PubMedCrossRef Buhmann C, Glauche V, Sturenburg HJ, Oechsner M, Weiller C, Buchel C (2003) Pharmacologically modulated fMRI cortical responsiveness to levodopa in drug-naive hemiparkinsonian patients. Brain 126:451–461PubMedCrossRef
13.
go back to reference Tessa C, Lucetti C, Diciotti S, Baldacci F, Paoli L, Cecchi P, Giannelli M, Ginestroni A, Del Dotto P, Ceravolo R, Vignali C, Bonuccelli U, Mascalchi M (2010) Decreased and increased cortical activation coexist in de-novo Parkinson’s disease. Exp Neurol 224:299–306 Tessa C, Lucetti C, Diciotti S, Baldacci F, Paoli L, Cecchi P, Giannelli M, Ginestroni A, Del Dotto P, Ceravolo R, Vignali C, Bonuccelli U, Mascalchi M (2010) Decreased and increased cortical activation coexist in de-novo Parkinson’s disease. Exp Neurol 224:299–306
14.
go back to reference Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, Bozzao L, Berry I, Montastruc JL, Chollet F, Rascol O (2000) Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain 123:394–403PubMedCrossRef Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, Bozzao L, Berry I, Montastruc JL, Chollet F, Rascol O (2000) Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain 123:394–403PubMedCrossRef
15.
go back to reference Haslinger B, Erhard P, Kampfe N, Boecker H, Rummeny E, Schwaiger M, Conrad B, Ceballos-Baumann AO (2001) Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain 124:558–570PubMedCrossRef Haslinger B, Erhard P, Kampfe N, Boecker H, Rummeny E, Schwaiger M, Conrad B, Ceballos-Baumann AO (2001) Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain 124:558–570PubMedCrossRef
16.
go back to reference Wu T, Hallet M (2005) A functional MRI study of automatic movements in patients with Parkinson’s disease. Brain 128:2250–2259PubMedCrossRef Wu T, Hallet M (2005) A functional MRI study of automatic movements in patients with Parkinson’s disease. Brain 128:2250–2259PubMedCrossRef
17.
go back to reference Eckert T, Peschel T, Heinze HJ, Rotte M (2006) Increased pre-SMA activation in early PD patients during simple self-initiated hand movements. J Neurol 253:199–207PubMedCrossRef Eckert T, Peschel T, Heinze HJ, Rotte M (2006) Increased pre-SMA activation in early PD patients during simple self-initiated hand movements. J Neurol 253:199–207PubMedCrossRef
18.
go back to reference Moraschi M, Giulietti G, Giove F, Guardati M, Garreffa G, Modugno N, Colonnese C, Maraviglia B (2010) fMRI study of motor cortex activity modulation in early Parkinson’s disease. Magn Reson Imaging 28:1152–1158PubMedCrossRef Moraschi M, Giulietti G, Giove F, Guardati M, Garreffa G, Modugno N, Colonnese C, Maraviglia B (2010) fMRI study of motor cortex activity modulation in early Parkinson’s disease. Magn Reson Imaging 28:1152–1158PubMedCrossRef
19.
go back to reference Peters S, Suchan B, Rusin J, Daum J, Kster O, Przuntek H, Muller T, Schmid G (2003) Apomorphine reduces BOLD signal in fMRI during voluntary movement in parkinsonian patients. Neuroreport 14:809–812PubMedCrossRef Peters S, Suchan B, Rusin J, Daum J, Kster O, Przuntek H, Muller T, Schmid G (2003) Apomorphine reduces BOLD signal in fMRI during voluntary movement in parkinsonian patients. Neuroreport 14:809–812PubMedCrossRef
20.
go back to reference Dagher A, Nagano-Saito A (2007) Functional and anatomical magnetic resonance imaging in Parkinson’s disease. Mol Imaging Biol 9:234–242PubMedCrossRef Dagher A, Nagano-Saito A (2007) Functional and anatomical magnetic resonance imaging in Parkinson’s disease. Mol Imaging Biol 9:234–242PubMedCrossRef
21.
go back to reference Gibb WRG, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752PubMedCrossRef Gibb WRG, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752PubMedCrossRef
22.
go back to reference Fahn S, Elton R, the members of the Unified Parkinson's Disease Rating Scale Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D (eds) Recent developments in Parkinson’s disease. MacMillan, New York, pp 153–163 Fahn S, Elton R, the members of the Unified Parkinson's Disease Rating Scale Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D (eds) Recent developments in Parkinson’s disease. MacMillan, New York, pp 153–163
23.
go back to reference Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMed Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMed
24.
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRef Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRef
25.
go back to reference Saini S, DeStefano N, Smith S, Guidi L, Amato MP, Federico A, Matthews PM (2004) Altered cerebellar functional connectivity mediates potential adaptive plasticity in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 75:840–846PubMedCrossRef Saini S, DeStefano N, Smith S, Guidi L, Amato MP, Federico A, Matthews PM (2004) Altered cerebellar functional connectivity mediates potential adaptive plasticity in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 75:840–846PubMedCrossRef
26.
go back to reference Diciotti S, Cecchi P, Ginestroni A, Mazzoni LN, Pesaresi I, Lombardo S, Boni E, Cosottini M, Soricelli A, De Stefano N, Mascalchi M (2010) MR-compatible device for monitoring hand tracing and writing tasks in fMRI with an application to healthy subjects. Conc Magn Reson Imaging – Part A 36A:139–152 Diciotti S, Cecchi P, Ginestroni A, Mazzoni LN, Pesaresi I, Lombardo S, Boni E, Cosottini M, Soricelli A, De Stefano N, Mascalchi M (2010) MR-compatible device for monitoring hand tracing and writing tasks in fMRI with an application to healthy subjects. Conc Magn Reson Imaging – Part A 36A:139–152
27.
go back to reference Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17:825–841PubMedCrossRef Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17:825–841PubMedCrossRef
29.
go back to reference Woolrich W, Ripley BD, Brady JM, Smith SM (2001) Temporal autocorrelation in univariate linear modelling of FMRI data. NeuroImage 14:1370–1386PubMedCrossRef Woolrich W, Ripley BD, Brady JM, Smith SM (2001) Temporal autocorrelation in univariate linear modelling of FMRI data. NeuroImage 14:1370–1386PubMedCrossRef
30.
go back to reference Worsley KJ (2001) Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM (eds), Functional MRI: an introduction to methods. OUP Worsley KJ (2001) Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM (eds), Functional MRI: an introduction to methods. OUP
31.
go back to reference Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156PubMedCrossRef Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156PubMedCrossRef
32.
go back to reference Andersson LR, Jenkinson M, Smith SM (2007) Non-linear optimisation. FMRIB technical report TR07JA1 Andersson LR, Jenkinson M, Smith SM (2007) Non-linear optimisation. FMRIB technical report TR07JA1
33.
go back to reference Andersson LR, Jenkinson M, Smith SM (2007) Non-linear registration, aka spatial normalization. FMRIB technical report TR07JA2 Andersson LR, Jenkinson M, Smith SM (2007) Non-linear registration, aka spatial normalization. FMRIB technical report TR07JA2
34.
go back to reference Beckmann C, Jenkinson M, Smith SM (2003) General multi-level linear modelling for group analysis in FMRI. NeuroImage 20:1052–1063PubMedCrossRef Beckmann C, Jenkinson M, Smith SM (2003) General multi-level linear modelling for group analysis in FMRI. NeuroImage 20:1052–1063PubMedCrossRef
35.
go back to reference Woolrich MW, Behrens TEJ, Beckmann CF, Jenkinson M, Smith SM (2004) Multi-level linear modelling for FMRI group analysis using Bayesian inference. NeuroImage 21:1732–1747PubMedCrossRef Woolrich MW, Behrens TEJ, Beckmann CF, Jenkinson M, Smith SM (2004) Multi-level linear modelling for FMRI group analysis using Bayesian inference. NeuroImage 21:1732–1747PubMedCrossRef
36.
37.
go back to reference Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289PubMedCrossRef Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289PubMedCrossRef
38.
go back to reference Ginestroni A, Diciotti S, Cecchi P, Pesaresi I, Tessa C, Giannelli M, Della Nave R, Salvatore E, Salvi F, Dotti MT, Piacentini S, Soricelli A, Cosottini M, De Stefano N, Mascalchi M (2011) Neurodegeneration in Friedreich’s ataxia is associated with a mixed activation pattern of the brain. A fMRI study. Hum Brain Mapp. doi: 10.1002/hbm.21319. Accessed 14 Jun 2011 Ginestroni A, Diciotti S, Cecchi P, Pesaresi I, Tessa C, Giannelli M, Della Nave R, Salvatore E, Salvi F, Dotti MT, Piacentini S, Soricelli A, Cosottini M, De Stefano N, Mascalchi M (2011) Neurodegeneration in Friedreich’s ataxia is associated with a mixed activation pattern of the brain. A fMRI study. Hum Brain Mapp. doi: 10.​1002/​hbm.​21319. Accessed 14 Jun 2011
39.
go back to reference Schlaug G, Sanes JN, Thangaraj V, Darby DG, Jancke L, Edelman RR, Warach S (1996) Cerebral activations covaries with movement rate. Neuroreport 7:879–883PubMedCrossRef Schlaug G, Sanes JN, Thangaraj V, Darby DG, Jancke L, Edelman RR, Warach S (1996) Cerebral activations covaries with movement rate. Neuroreport 7:879–883PubMedCrossRef
40.
go back to reference Rao SM, Bandettini PA, Binder JR, Bobholz JA, Hammeke TA, Stein EA, Hyde JS (1996) Relationship between finger movement rate and functional magnetic resonance signal change in human primary motor cortex. J Cereb Blood Flow Metab 16:1250–1254PubMedCrossRef Rao SM, Bandettini PA, Binder JR, Bobholz JA, Hammeke TA, Stein EA, Hyde JS (1996) Relationship between finger movement rate and functional magnetic resonance signal change in human primary motor cortex. J Cereb Blood Flow Metab 16:1250–1254PubMedCrossRef
41.
go back to reference Jancke L, Peters M, Schlaug G, Posse S, Steinmetz H, Muller-Gartner HM (1998) Differential magnetic resonance signal change in human sensorimotor cortex to finger movements of different rate of the dominant hand and subdominant hand. Brain Res Cogn Brain Res 6:279–284PubMedCrossRef Jancke L, Peters M, Schlaug G, Posse S, Steinmetz H, Muller-Gartner HM (1998) Differential magnetic resonance signal change in human sensorimotor cortex to finger movements of different rate of the dominant hand and subdominant hand. Brain Res Cogn Brain Res 6:279–284PubMedCrossRef
42.
go back to reference Deiber MP, Honda M, Ibanez V, Sadato N, Hallett M (1999) Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. J Neurophysiol 81:3065–3077PubMed Deiber MP, Honda M, Ibanez V, Sadato N, Hallett M (1999) Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. J Neurophysiol 81:3065–3077PubMed
43.
go back to reference Riecker A, Wildgruber D, Mathiak K, Grodd W, Ackermann H (2003) Parametric analysis of rate-dependent hemodynamic response functions of cortical and subcortical brain structures during auditorily cued finger tapping: a fMRI study. NeuroImage 18:731–739PubMedCrossRef Riecker A, Wildgruber D, Mathiak K, Grodd W, Ackermann H (2003) Parametric analysis of rate-dependent hemodynamic response functions of cortical and subcortical brain structures during auditorily cued finger tapping: a fMRI study. NeuroImage 18:731–739PubMedCrossRef
44.
go back to reference Lutz K, Koeneke S, Wustenberg T, Jancke L (2005) Asymmetry of cortical activation during maximum and convenient tapping speed. Neurosci Lett 373:61–66PubMedCrossRef Lutz K, Koeneke S, Wustenberg T, Jancke L (2005) Asymmetry of cortical activation during maximum and convenient tapping speed. Neurosci Lett 373:61–66PubMedCrossRef
45.
go back to reference Cerasa A, Hagberg GE, Peppe A, Bianciardi M, Gioia MC, Costa A, Castriota-Scanderbeg A, Caltagirone C, Sabatini U (2006) Functional changes in the activity of cerebellum and frontostriatal regions during externally and internally timed movement in Parkinson’s disease. Brain Res Bull 71:259–269PubMedCrossRef Cerasa A, Hagberg GE, Peppe A, Bianciardi M, Gioia MC, Costa A, Castriota-Scanderbeg A, Caltagirone C, Sabatini U (2006) Functional changes in the activity of cerebellum and frontostriatal regions during externally and internally timed movement in Parkinson’s disease. Brain Res Bull 71:259–269PubMedCrossRef
46.
go back to reference Yu H, Sternad D, Corcos DM, Vaillancourt DE (2007) Role of iperactive cerebellum and motor cortex in Parkinson’s disease. NeuroImage 35:222–233PubMedCrossRef Yu H, Sternad D, Corcos DM, Vaillancourt DE (2007) Role of iperactive cerebellum and motor cortex in Parkinson’s disease. NeuroImage 35:222–233PubMedCrossRef
47.
go back to reference Spraker MB, Prodoehl J, Corcos DM, Comella CL, Vaillancourt DE (2010) Basal ganglia hypoactivity during grip force in drug-naive Parkinson’s disease. Hum Brain Mapp 31:1928–1941PubMedCrossRef Spraker MB, Prodoehl J, Corcos DM, Comella CL, Vaillancourt DE (2010) Basal ganglia hypoactivity during grip force in drug-naive Parkinson’s disease. Hum Brain Mapp 31:1928–1941PubMedCrossRef
48.
go back to reference Taniwaki T, Okajama A, Yoshiura T, Togao O, Nakamura Y, Yamasaki T, Ogata K, Shigeto H, Ohyagy Y, Kira J, Tobimatsu S (2006) Functional network of the basal ganglia and cerebellar motor loops in vivo: different activation patterns between self-initiated and externally triggered movements. NeuroImage 31:745–753PubMedCrossRef Taniwaki T, Okajama A, Yoshiura T, Togao O, Nakamura Y, Yamasaki T, Ogata K, Shigeto H, Ohyagy Y, Kira J, Tobimatsu S (2006) Functional network of the basal ganglia and cerebellar motor loops in vivo: different activation patterns between self-initiated and externally triggered movements. NeuroImage 31:745–753PubMedCrossRef
49.
go back to reference Lewis MM, Slagle CG, Smith AB, Truong Y, Bai P, McKeown MJ, Mailman RB, Belger A, Huang X (2007) Task specific influences of Parkinson’s disease on the striato-thalamo-cortical and cerebello-thalamo-cortical motor circuitries. Neuroscience 147:224–235PubMedCrossRef Lewis MM, Slagle CG, Smith AB, Truong Y, Bai P, McKeown MJ, Mailman RB, Belger A, Huang X (2007) Task specific influences of Parkinson’s disease on the striato-thalamo-cortical and cerebello-thalamo-cortical motor circuitries. Neuroscience 147:224–235PubMedCrossRef
Metadata
Title
Hypoactivation of the primary sensorimotor cortex in de novo Parkinson’s disease
A motor fMRI study under controlled conditions
Authors
Carlo Tessa
Claudio Lucetti
Stefano Diciotti
Lorenzo Paoli
Paolo Cecchi
Marco Giannelli
Filippo Baldacci
Andrea Ginestroni
Claudio Vignali
Mario Mascalchi
Ubaldo Bonuccelli
Publication date
01-03-2012
Publisher
Springer-Verlag
Published in
Neuroradiology / Issue 3/2012
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-011-0955-y

Other articles of this Issue 3/2012

Neuroradiology 3/2012 Go to the issue